Skip to main content
Top
Published in: Calcified Tissue International 5/2010

01-05-2010

Negative Association between Metabolic Syndrome and Bone Mineral Density in Koreans, Especially in Men

Authors: Ha Young Kim, Jae Won Choe, Hong Kyu Kim, Sung Jin Bae, Beom Jun Kim, Seung Hun Lee, Jung-Min Koh, Ki Ok Han, Hyoung Moo Park, Ghi Su Kim

Published in: Calcified Tissue International | Issue 5/2010

Login to get access

Abstract

Cardiovascular disease and osteoporosis are thought to share common risk factors, and metabolic syndrome (MS) is composed of major risk factors for cardiovascular disease. This study was performed to investigate the relationships between specific MS components and bone mineral density (BMD). BMD was measured at the femoral neck of Korean men aged 40 years or more (n = 1,780) and postmenopausal women (n = 1,108) using dual-energy X-ray absorptiometry. We identified subjects with MS as defined by two criteria, International Diabetes Federation (IDF) and American Heart Association/National Heart, Lung, and Blood Institute (AHA/NHLBI). Body fat and lean mass were measured via bioimpedance analysis. The prevalence of MS was 19.8% and 7.7% in men and 20.8% and 11.6% in postmenopausal women according to the AHA/NHLBI definition and the IDF definition, respectively. After multivariate adjustment, femoral neck BMD was significantly lower in subjects with MS regardless of diagnostic criteria. BMD decreased as the number of MS components increased (P < 0.001 for trends in both sexes). Among MS components, waist circumference was the most important factor in this negative association. When multiple linear regression models were applied to each 5-kg weight stratum to test for a linear trend, waist circumference and fat mass were negatively associated with BMD and lean mass was positively associated with BMD in men but not in women. MS was associated with a lower BMD in Korean men and postmenopausal women, suggesting that visceral fat may lead to bone loss, especially in men.
Literature
1.
go back to reference Schulz E, Arfai K, Liu X, Sayre J, Gilsanz V (2004) Aortic calcification and the risk of osteoporosis and fractures. J Clin Endocrinol Metab 89:4246–4253CrossRefPubMed Schulz E, Arfai K, Liu X, Sayre J, Gilsanz V (2004) Aortic calcification and the risk of osteoporosis and fractures. J Clin Endocrinol Metab 89:4246–4253CrossRefPubMed
2.
go back to reference Samelson EJ, Kiel DP, Broe KE, Zhang Y, Cupples LA, Hannan MT, Wilson PW, Levy D, Williams SA, Vaccarino V (2004) Metacarpal cortical area and risk of coronary heart disease: the Framingham Study. Am J Epidemiol 159:589–595CrossRefPubMed Samelson EJ, Kiel DP, Broe KE, Zhang Y, Cupples LA, Hannan MT, Wilson PW, Levy D, Williams SA, Vaccarino V (2004) Metacarpal cortical area and risk of coronary heart disease: the Framingham Study. Am J Epidemiol 159:589–595CrossRefPubMed
3.
go back to reference Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 20:1912–1920CrossRefPubMed Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 20:1912–1920CrossRefPubMed
4.
go back to reference Szulc P, Samelson EJ, Kiel DP, Delmas PD (2009) Increased bone resorption is associated with increased risk of cardiovascular events in men—the MINOS Study. J Bone Miner Res 24:2023–2031CrossRefPubMed Szulc P, Samelson EJ, Kiel DP, Delmas PD (2009) Increased bone resorption is associated with increased risk of cardiovascular events in men—the MINOS Study. J Bone Miner Res 24:2023–2031CrossRefPubMed
5.
go back to reference Szulc P, Garnero P, Claustrat B, Marchand F, Duboeuf F, Delmas PD (2002) Increased bone resorption in moderate smokers with low body weight: the Minos study. J Clin Endocrinol Metab 87:666–674CrossRefPubMed Szulc P, Garnero P, Claustrat B, Marchand F, Duboeuf F, Delmas PD (2002) Increased bone resorption in moderate smokers with low body weight: the Minos study. J Clin Endocrinol Metab 87:666–674CrossRefPubMed
6.
go back to reference Fink HA, Ewing SK, Ensrud KE, Barrett-Connor E, Taylor BC, Cauley JA, Orwoll ES (2006) Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men. J Clin Endocrinol Metab 91:3908–3915CrossRefPubMed Fink HA, Ewing SK, Ensrud KE, Barrett-Connor E, Taylor BC, Cauley JA, Orwoll ES (2006) Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men. J Clin Endocrinol Metab 91:3908–3915CrossRefPubMed
7.
go back to reference Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab 93:1952–1958CrossRefPubMed Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab 93:1952–1958CrossRefPubMed
8.
go back to reference Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O’Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297CrossRefPubMed Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O’Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297CrossRefPubMed
9.
go back to reference Kinjo M, Setoguchi S, Solomon DH (2007) Bone mineral density in adults with the metabolic syndrome: analysis in a population-based U.S. sample. J Clin Endocrinol Metab 92:4161–4164CrossRefPubMed Kinjo M, Setoguchi S, Solomon DH (2007) Bone mineral density in adults with the metabolic syndrome: analysis in a population-based U.S. sample. J Clin Endocrinol Metab 92:4161–4164CrossRefPubMed
10.
go back to reference Ahmed LA, Schirmer H, Berntsen GK, Fonnebo V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int 17:426–432CrossRefPubMed Ahmed LA, Schirmer H, Berntsen GK, Fonnebo V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int 17:426–432CrossRefPubMed
11.
go back to reference von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int 18:1337–1344CrossRef von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int 18:1337–1344CrossRef
12.
go back to reference Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431CrossRefPubMed Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431CrossRefPubMed
13.
go back to reference Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10CrossRefPubMed Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10CrossRefPubMed
14.
go back to reference Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complications 17:39–58CrossRefPubMed Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complications 17:39–58CrossRefPubMed
15.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752CrossRefPubMed Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752CrossRefPubMed
16.
go back to reference Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062CrossRefPubMed Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062CrossRefPubMed
17.
go back to reference Jukka AS (2003) Body composition assessment with segmental multifrequency bioimpedance method. J Sports Sci Med 2(suppl 3):1–29 Jukka AS (2003) Body composition assessment with segmental multifrequency bioimpedance method. J Sports Sci Med 2(suppl 3):1–29
18.
go back to reference Malavolti M, Mussi C, Poli M, Fantuzzi AL, Salvioli G, Battistini N, Bedogni G (2003) Cross-calibration of eight-polar bioelectrical impedance analysis versus dual-energy X-ray absorptiometry for the assessment of total and appendicular body composition in healthy subjects aged 21–82 years. Ann Hum Biol 30:380–391CrossRefPubMed Malavolti M, Mussi C, Poli M, Fantuzzi AL, Salvioli G, Battistini N, Bedogni G (2003) Cross-calibration of eight-polar bioelectrical impedance analysis versus dual-energy X-ray absorptiometry for the assessment of total and appendicular body composition in healthy subjects aged 21–82 years. Ann Hum Biol 30:380–391CrossRefPubMed
19.
go back to reference Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646CrossRefPubMed Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646CrossRefPubMed
20.
go back to reference Hsu YH, Venners SA, Terwedow HA, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML, Rosen CJ, Xu X (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, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML, Rosen CJ, Xu X (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
21.
go back to reference Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280:E745–E751PubMed Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280:E745–E751PubMed
22.
go back to reference Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949CrossRefPubMed Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949CrossRefPubMed
23.
go back to reference Jilka RL, Hangoc G, Girasole G, Passeri G, Williams DC, Abrams JS, Boyce B, Broxmeyer H, Manolagas SC (1992) Increased osteoclast development after estrogen loss: mediation by interleukin-6. Science 257:88–91CrossRefPubMed Jilka RL, Hangoc G, Girasole G, Passeri G, Williams DC, Abrams JS, Boyce B, Broxmeyer H, Manolagas SC (1992) Increased osteoclast development after estrogen loss: mediation by interleukin-6. Science 257:88–91CrossRefPubMed
24.
go back to reference Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305–311CrossRefPubMed Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305–311CrossRefPubMed
25.
go back to reference Nanes MS (2003) Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene 321:1–15CrossRefPubMed Nanes MS (2003) Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene 321:1–15CrossRefPubMed
26.
go back to reference Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR (1986) Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319:516–518CrossRefPubMed Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR (1986) Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319:516–518CrossRefPubMed
27.
go back to reference Salamone LM, Whiteside T, Friberg D, Epstein RS, Kuller LH, Cauley JA (1998) Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausal women. Calcif Tissue Int 63:466–470CrossRefPubMed Salamone LM, Whiteside T, Friberg D, Epstein RS, Kuller LH, Cauley JA (1998) Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausal women. Calcif Tissue Int 63:466–470CrossRefPubMed
28.
go back to reference Cohen-Solal ME, Graulet AM, Denne MA, Gueris J, Baylink D, de Vernejoul MC (1993) Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab 77:1648–1653CrossRefPubMed Cohen-Solal ME, Graulet AM, Denne MA, Gueris J, Baylink D, de Vernejoul MC (1993) Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab 77:1648–1653CrossRefPubMed
29.
go back to reference Scheidt-Nave C, Bismar H, Leidig-Bruckner G, Woitge H, Seibel MJ, Ziegler R, Pfeilschifter J (2001) Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab 86:2032–2042CrossRefPubMed Scheidt-Nave C, Bismar H, Leidig-Bruckner G, Woitge H, Seibel MJ, Ziegler R, Pfeilschifter J (2001) Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab 86:2032–2042CrossRefPubMed
30.
go back to reference Kuk JL, Lee S, Heymsfield SB, Ross R (2005) Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 81:1330–1334PubMed Kuk JL, Lee S, Heymsfield SB, Ross R (2005) Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 81:1330–1334PubMed
31.
go back to reference Schreiner PJ, Terry JG, Evans GW, Hinson WH, Crouse JR 3rd, Heiss G (1996) Sex-specific associations of magnetic resonance imaging-derived intra-abdominal and subcutaneous fat areas with conventional anthropometric indices. The Atherosclerosis Risk in Communities Study. Am J Epidemiol 144:335–345PubMed Schreiner PJ, Terry JG, Evans GW, Hinson WH, Crouse JR 3rd, Heiss G (1996) Sex-specific associations of magnetic resonance imaging-derived intra-abdominal and subcutaneous fat areas with conventional anthropometric indices. The Atherosclerosis Risk in Communities Study. Am J Epidemiol 144:335–345PubMed
32.
go back to reference Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Despres JP (1993) Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 58:463–467PubMed Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Despres JP (1993) Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 58:463–467PubMed
33.
go back to reference Jankowska EA, Rogucka E, Medras M (2001) Are general obesity and visceral adiposity in men linked to reduced bone mineral content resulting from normal ageing? A population-based study. Andrologia 33:384–389CrossRefPubMed Jankowska EA, Rogucka E, Medras M (2001) Are general obesity and visceral adiposity in men linked to reduced bone mineral content resulting from normal ageing? A population-based study. Andrologia 33:384–389CrossRefPubMed
34.
go back to reference Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25:165–171CrossRefPubMed Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25:165–171CrossRefPubMed
35.
go back to reference Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084PubMed Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084PubMed
36.
go back to reference Hanley DA, Brown JP, Tenenhouse A, Olszynski WP, Ioannidis G, Berger C, Prior JC, Pickard L, Murray TM, Anastassiades T, Kirkland S, Joyce C, Joseph L, Papaioannou A, Jackson SA, Poliquin S, Adachi JD (2003) Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res 18:784–790CrossRefPubMed Hanley DA, Brown JP, Tenenhouse A, Olszynski WP, Ioannidis G, Berger C, Prior JC, Pickard L, Murray TM, Anastassiades T, Kirkland S, Joyce C, Joseph L, Papaioannou A, Jackson SA, Poliquin S, Adachi JD (2003) Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res 18:784–790CrossRefPubMed
37.
go back to reference Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F (1986) Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 44:739–746PubMed Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F (1986) Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 44:739–746PubMed
Metadata
Title
Negative Association between Metabolic Syndrome and Bone Mineral Density in Koreans, Especially in Men
Authors
Ha Young Kim
Jae Won Choe
Hong Kyu Kim
Sung Jin Bae
Beom Jun Kim
Seung Hun Lee
Jung-Min Koh
Ki Ok Han
Hyoung Moo Park
Ghi Su Kim
Publication date
01-05-2010
Publisher
Springer-Verlag
Published in
Calcified Tissue International / Issue 5/2010
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-010-9347-2

Other articles of this Issue 5/2010

Calcified Tissue International 5/2010 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.