Skip to main content
Top
Published in: Osteoporosis International 1/2017

01-01-2017 | Original Article

Discordance between fat mass index and body mass index is associated with reduced bone mineral density in women but not in men: the Busselton Healthy Ageing Study

Authors: K. Zhu, M. Hunter, A. James, E. M. Lim, B. R. Cooke, J. P. Walsh

Published in: Osteoporosis International | Issue 1/2017

Login to get access

Abstract

Summary

The obesity-BMD relationship is complex. In 3045 middle-aged adults, we found that in women (but not men) with discordant fat mass index (FMI)/BMI categories, higher body fat for BMI was associated with lower BMD, suggesting that increased fat mass without an accompanying increase in lean mass may be deleterious to bone.

Introduction

The relationship between obesity and BMD is complex. FMI (fat mass (kg) / height (m)2) is a more accurate measure of fatness than BMI, and depending on body composition, some individuals have discordant BMI/FMI categories. We examined associations between FMI, BMI and BMD in participants in the Busselton Healthy Ageing Study.

Methods

Body composition and BMD of the hip, spine and total body were measured using DXA in 3045 participants (1644 females) aged 45–67 years. Using standard BMI/FMI categories, the participants were classified as underweight/fat deficit, normal, overweight/excess fat, obese I and obese II–III.

Results

BMI and FMI categories were concordant in 77.3 % of females and 71.2 % of males. There were 12.9 % females and 13.2 % males in a higher FMI than BMI category (high body fat for BMI), whereas 9.8 % females and 15.6 % males were in a lower category (low body fat for BMI). Females with high body fat for BMI had significantly lower covariate-adjusted BMD at the femoral neck, total hip and total body (differences of 3.8, 5.1 and 2.6 %, respectively, all P < 0.05) than females with low body fat for BMI and lower total body BMD than women with concordant FMI/BMI (by 1.4 %, P = 0.04). In males, BMD did not differ significantly between those who were concordant or discordant for FMI/BMI categories.

Conclusion

In women (but not men) with discordant FMI/BMI categories, higher body fat for BMI was associated with lower BMD, suggesting that increased fat mass without an accompanying increase in lean mass may be deleterious to bone.
Literature
1.
go back to reference Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573CrossRefPubMed Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573CrossRefPubMed
2.
go back to reference Lloyd JT, Alley DE, Hawkes WG, Hochberg MC, Waldstein SR, Orwig DL (2014) Body mass index is positively associated with bone mineral density in US older adults. Arch Osteoporos 9:175CrossRefPubMed Lloyd JT, Alley DE, Hawkes WG, Hochberg MC, Waldstein SR, Orwig DL (2014) Body mass index is positively associated with bone mineral density in US older adults. Arch Osteoporos 9:175CrossRefPubMed
3.
go back to reference Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng HW (2008) Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 23:17–29CrossRefPubMed Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng HW (2008) Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 23:17–29CrossRefPubMed
5.
go back to reference Prieto-Alhambra D, Premaor MO, Fina Aviles F, Hermosilla E, Martinez-Laguna D, Carbonell-Abella C, Nogues X, Compston JE, Diez-Perez A (2012) The association between fracture and obesity is site-dependent: a population-based study in postmenopausal women. J Bone Miner Res 27:294–300CrossRefPubMed Prieto-Alhambra D, Premaor MO, Fina Aviles F, Hermosilla E, Martinez-Laguna D, Carbonell-Abella C, Nogues X, Compston JE, Diez-Perez A (2012) The association between fracture and obesity is site-dependent: a population-based study in postmenopausal women. J Bone Miner Res 27:294–300CrossRefPubMed
6.
go back to reference Gjesdal CG, Halse JI, Eide GE, Brun JG, Tell GS (2008) Impact of lean mass and fat mass on bone mineral density: the Hordaland Health Study. Maturitas 59:191–200CrossRefPubMed Gjesdal CG, Halse JI, Eide GE, Brun JG, Tell GS (2008) Impact of lean mass and fat mass on bone mineral density: the Hordaland Health Study. Maturitas 59:191–200CrossRefPubMed
7.
go back to reference Bachmann KN, Bruno AG, Bredella MA et al (2016) Vertebral strength and estimated fracture risk across the BMI spectrum in women. J Bone Miner Res 31:281–288CrossRefPubMed Bachmann KN, Bruno AG, Bredella MA et al (2016) Vertebral strength and estimated fracture risk across the BMI spectrum in women. J Bone Miner Res 31:281–288CrossRefPubMed
8.
go back to reference Douchi T, Kuwahata R, Matsuo T, Uto H, Oki T, Nagata Y (2003) Relative contribution of lean and fat mass component to bone mineral density in males. J Bone Miner Metab 21:17–21CrossRefPubMed Douchi T, Kuwahata R, Matsuo T, Uto H, Oki T, Nagata Y (2003) Relative contribution of lean and fat mass component to bone mineral density in males. J Bone Miner Metab 21:17–21CrossRefPubMed
9.
go back to reference Douchi T, Matsuo T, Uto H, Kuwahata T, Oki T, Nagata Y (2003) Lean body mass and bone mineral density in physically exercising postmenopausal women. Maturitas 45:185–190CrossRefPubMed Douchi T, Matsuo T, Uto H, Kuwahata T, Oki T, Nagata Y (2003) Lean body mass and bone mineral density in physically exercising postmenopausal women. Maturitas 45:185–190CrossRefPubMed
10.
go back to reference Liu JM, Zhao HY, Ning G, Zhao YJ, Zhang LZ, Sun LH, Xu MY, Chen JL (2004) Relationship between body composition and bone mineral density in healthy young and premenopausal Chinese women. Osteoporos Int 15:238–242CrossRefPubMed Liu JM, Zhao HY, Ning G, Zhao YJ, Zhang LZ, Sun LH, Xu MY, Chen JL (2004) Relationship between body composition and bone mineral density in healthy young and premenopausal Chinese women. Osteoporos Int 15:238–242CrossRefPubMed
11.
go back to reference Reid IR, Evans MC, Ames RW (1994) Volumetric bone density of the lumbar spine is related to fat mass but not lean mass in normal postmenopausal women. Osteoporos Int 4:362–367CrossRefPubMed Reid IR, Evans MC, Ames RW (1994) Volumetric bone density of the lumbar spine is related to fat mass but not lean mass in normal postmenopausal women. Osteoporos Int 4:362–367CrossRefPubMed
12.
go back to reference Reid IR, Ames R, Evans MC, Sharpe S, Gamble G, France JT, Lim TM, Cundy TF (1992) Determinants of total body and regional bone mineral density in normal postmenopausal women—a key role for fat mass. J Clin Endocrinol Metab 75:45–51PubMed Reid IR, Ames R, Evans MC, Sharpe S, Gamble G, France JT, Lim TM, Cundy TF (1992) Determinants of total body and regional bone mineral density in normal postmenopausal women—a key role for fat mass. J Clin Endocrinol Metab 75:45–51PubMed
13.
go back to reference Gnudi S, Sitta E, Fiumi N (2007) Relationship between body composition and bone mineral density in women with and without osteoporosis: relative contribution of lean and fat mass. J Bone Miner Metab 25:326–332CrossRefPubMed Gnudi S, Sitta E, Fiumi N (2007) Relationship between body composition and bone mineral density in women with and without osteoporosis: relative contribution of lean and fat mass. J Bone Miner Metab 25:326–332CrossRefPubMed
14.
go back to reference Ijuin M, Douchi T, Matsuo T, Yamamoto S, Uto H, Nagata Y (2002) Difference in the effects of body composition on bone mineral density between pre- and postmenopausal women. Maturitas 43:239–244CrossRefPubMed Ijuin M, Douchi T, Matsuo T, Yamamoto S, Uto H, Nagata Y (2002) Difference in the effects of body composition on bone mineral density between pre- and postmenopausal women. Maturitas 43:239–244CrossRefPubMed
15.
go back to reference Zhu K, Briffa K, Smith A, Mountain J, Briggs AM, Lye S, Pennell C, Straker L, Walsh JP (2014) Gender differences in the relationships between lean body mass, fat mass and peak bone mass in young adults. Osteoporos Int 25:1563–1570CrossRefPubMed Zhu K, Briffa K, Smith A, Mountain J, Briggs AM, Lye S, Pennell C, Straker L, Walsh JP (2014) Gender differences in the relationships between lean body mass, fat mass and peak bone mass in young adults. Osteoporos Int 25:1563–1570CrossRefPubMed
17.
go back to reference Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72:694–701PubMed Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72:694–701PubMed
18.
go back to reference Zhu K, Hunter M, James A, Lim EM, Walsh JP (2015) Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: the Busselton Healthy Ageing Study. Bone 74:146–152CrossRefPubMed Zhu K, Hunter M, James A, Lim EM, Walsh JP (2015) Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: the Busselton Healthy Ageing Study. Bone 74:146–152CrossRefPubMed
19.
go back to reference James A, Hunter M, Straker L et al (2013) Rationale, design and methods for a community-based study of clustering and cumulative effects of chronic disease processes and their effects on ageing: the Busselton Healthy Ageing Study. BMC Public Health 13:936CrossRefPubMedPubMedCentral James A, Hunter M, Straker L et al (2013) Rationale, design and methods for a community-based study of clustering and cumulative effects of chronic disease processes and their effects on ageing: the Busselton Healthy Ageing Study. BMC Public Health 13:936CrossRefPubMedPubMedCentral
20.
go back to reference WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO Consultation. WHO Technical Report Series 894. World Health Organization, Geneva WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO Consultation. WHO Technical Report Series 894. World Health Organization, Geneva
22.
go back to reference Cooke DJ, Cooke B, Bell D, Vasikaran S, Glendenning P (2015) ANNALS EXPRESS: C-3-epi-25-hydroxyvitamin D is universally present in neonatal Western Australian samples but is unlikely to contribute to diagnostic misclassification. Ann Clin Biochem. doi:10.1177/0004563215625693 PubMed Cooke DJ, Cooke B, Bell D, Vasikaran S, Glendenning P (2015) ANNALS EXPRESS: C-3-epi-25-hydroxyvitamin D is universally present in neonatal Western Australian samples but is unlikely to contribute to diagnostic misclassification. Ann Clin Biochem. doi:10.​1177/​0004563215625693​ PubMed
23.
go back to reference Hsu YH, Venners SA, Terwedow HA et al (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83:146–154PubMed Hsu YH, Venners SA, Terwedow HA et al (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83:146–154PubMed
24.
25.
go back to reference Tang ZH, Xiao P, Lei SF et al (2007) A bivariate whole-genome linkage scan suggests several shared genomic regions for obesity and osteoporosis. J Clin Endocrinol Metab 92:2751–2757CrossRefPubMed Tang ZH, Xiao P, Lei SF et al (2007) A bivariate whole-genome linkage scan suggests several shared genomic regions for obesity and osteoporosis. J Clin Endocrinol Metab 92:2751–2757CrossRefPubMed
26.
go back to reference David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, Jones DB, Vico L, Guignandon A (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148:2553–2562CrossRefPubMed David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, Jones DB, Vico L, Guignandon A (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148:2553–2562CrossRefPubMed
27.
go back to reference Colaianni G, Brunetti G, Faienza MF, Colucci S, Grano M (2014) Osteoporosis and obesity: role of Wnt pathway in human and murine models. World J Orthop 5:242–246CrossRefPubMedPubMedCentral Colaianni G, Brunetti G, Faienza MF, Colucci S, Grano M (2014) Osteoporosis and obesity: role of Wnt pathway in human and murine models. World J Orthop 5:242–246CrossRefPubMedPubMedCentral
28.
go back to reference Braun T, Schett G (2012) Pathways for bone loss in inflammatory disease. Curr Osteoporos Rep 10:101–108CrossRefPubMed Braun T, Schett G (2012) Pathways for bone loss in inflammatory disease. Curr Osteoporos Rep 10:101–108CrossRefPubMed
29.
go back to reference Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Harrington LM, Breggia A, Rosen CJ, Miller KK (2011) Determinants of bone mineral density in obese premenopausal women. Bone 48:748–754CrossRefPubMed Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Harrington LM, Breggia A, Rosen CJ, Miller KK (2011) Determinants of bone mineral density in obese premenopausal women. Bone 48:748–754CrossRefPubMed
30.
go back to reference Bolland MJ, Grey AB, Ames RW, Mason BH, Horne AM, Gamble GD, Reid IR (2006) Determinants of vitamin D status in older men living in a subtropical climate. Osteoporos Int 17:1742–1748CrossRefPubMed Bolland MJ, Grey AB, Ames RW, Mason BH, Horne AM, Gamble GD, Reid IR (2006) Determinants of vitamin D status in older men living in a subtropical climate. Osteoporos Int 17:1742–1748CrossRefPubMed
31.
go back to reference Bolland MJ, Grey AB, Ames RW, Horne AM, Gamble GD, Reid IR (2006) Fat mass is an important predictor of parathyroid hormone levels in postmenopausal women. Bone 38:317–321CrossRefPubMed Bolland MJ, Grey AB, Ames RW, Horne AM, Gamble GD, Reid IR (2006) Fat mass is an important predictor of parathyroid hormone levels in postmenopausal women. Bone 38:317–321CrossRefPubMed
33.
go back to reference St-Onge MP (2005) Relationship between body composition changes and changes in physical function and metabolic risk factors in aging. Curr Opin Clin Nutr Metab Care 8:523–528PubMed St-Onge MP (2005) Relationship between body composition changes and changes in physical function and metabolic risk factors in aging. Curr Opin Clin Nutr Metab Care 8:523–528PubMed
34.
35.
go back to reference Ilich JZ, Inglis JE, Kelly OJ, McGee DL (2015) Osteosarcopenic obesity is associated with reduced handgrip strength, walking abilities, and balance in postmenopausal women. Osteoporos Int 26:2587–2595CrossRefPubMed Ilich JZ, Inglis JE, Kelly OJ, McGee DL (2015) Osteosarcopenic obesity is associated with reduced handgrip strength, walking abilities, and balance in postmenopausal women. Osteoporos Int 26:2587–2595CrossRefPubMed
36.
go back to reference Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ (2012) Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr 96:1454–1464CrossRefPubMed Cermak NM, Res PT, de Groot LC, Saris WH, van Loon LJ (2012) Protein supplementation augments the adaptive response of skeletal muscle to resistance-type exercise training: a meta-analysis. Am J Clin Nutr 96:1454–1464CrossRefPubMed
38.
go back to reference Dimitri P, Bishop N, Walsh JS, Eastell R (2012) Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone 50:457–466CrossRefPubMed Dimitri P, Bishop N, Walsh JS, Eastell R (2012) Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone 50:457–466CrossRefPubMed
39.
go back to reference Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 307:491–497CrossRefPubMed Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA 307:491–497CrossRefPubMed
41.
go back to reference Yu EW, Thomas BJ, Brown JK, Finkelstein JS (2012) Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT. J Bone Miner Res 27:119–124CrossRefPubMed Yu EW, Thomas BJ, Brown JK, Finkelstein JS (2012) Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT. J Bone Miner Res 27:119–124CrossRefPubMed
Metadata
Title
Discordance between fat mass index and body mass index is associated with reduced bone mineral density in women but not in men: the Busselton Healthy Ageing Study
Authors
K. Zhu
M. Hunter
A. James
E. M. Lim
B. R. Cooke
J. P. Walsh
Publication date
01-01-2017
Publisher
Springer London
Published in
Osteoporosis International / Issue 1/2017
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-016-3710-8

Other articles of this Issue 1/2017

Osteoporosis International 1/2017 Go to the issue