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Published in: Journal of Bone and Mineral Metabolism 6/2013

01-11-2013 | Original Article

Association between metabolic syndrome and bone mineral density in Korea: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008

Authors: Taehun Kim, Sangshin Park, Yun-Suk Pak, Sangyoon Lee, Eun-Hee Lee

Published in: Journal of Bone and Mineral Metabolism | Issue 6/2013

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Abstract

Little is known regarding the exact relationship between osteoporosis and cardiovascular disease. Moreover, previous research on the relationships between components of metabolic syndrome (MetS) and bone mineral density (BMD) has primarily focused on women and older men; there have been few studies in younger men. We performed a cross-sectional study to assess whether MetS is associated with BMD in the femoral neck or lumbar spine in Korean adults. We further attempted to identify the MetS component, which is the most important factor in BMD. We performed a multiple regression analysis to analyze data on 2,989 subjects from the Fourth Korea National Health and Nutrition Examination Survey. We examined the association between MetS and individuals MetS components and BMD. After adjustment for age, height, weight, smoking status, alcohol consumption and exercise, waist circumference (WC) and diastolic blood pressure (DBP) showed independent negative associations with femoral neck and spine BMD in men in all age groups. Triglyceride concentration was also negatively associated with femoral neck BMD in younger men (<45 years). In premenopausal women, WC, DBP, and high-density lipoprotein cholesterol were negatively associated with spine BMD. In postmenopausal women, WC was negatively associated with femoral neck BMD. These results suggest that WC in men in all age groups may be the most important factor in bone mineral density.
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 89:4246–4253PubMedCrossRef Schulz E, Arfai K, Liu X, Sayre J, Gilsanz V (2004) Aortic calcification and the risk of osteoporosis and fractures. J Clin Endocrinol Metab 89:4246–4253PubMedCrossRef
2.
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 20:1912–1920PubMedCrossRef 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 20:1912–1920PubMedCrossRef
3.
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 24:2023–2031PubMedCrossRef 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 24:2023–2031PubMedCrossRef
4.
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 87:666–674PubMedCrossRef 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 87:666–674PubMedCrossRef
5.
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 91:3908–3915PubMedCrossRef 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 91:3908–3915PubMedCrossRef
6.
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 93:1952–1958PubMedCrossRef 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 93:1952–1958PubMedCrossRef
7.
go back to reference Almeida M, Han L, Martin-Millan M et al (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297PubMedCrossRef Almeida M, Han L, Martin-Millan M et al (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297PubMedCrossRef
8.
go back to reference Grundy SM, Cleeman JI, Daniels SR et al (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752PubMedCrossRef Grundy SM, Cleeman JI, Daniels SR et al (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752PubMedCrossRef
9.
go back to reference Dupuy AM, Jaussent I, Lacroux A, Durant R, Cristol JP, Delcourt C (2007) Waist circumference adds to the variance in plasma C-reactive protein levels in elderly patients with metabolic syndrome. Gerontology 53:329–339PubMedCrossRef Dupuy AM, Jaussent I, Lacroux A, Durant R, Cristol JP, Delcourt C (2007) Waist circumference adds to the variance in plasma C-reactive protein levels in elderly patients with metabolic syndrome. Gerontology 53:329–339PubMedCrossRef
10.
go back to reference Maggio M, Lauretani F, Ceda GP et al (2010) Estradiol and metabolic syndrome in older Italian men: The InCHIANTI Study. J Androl 31:155–162PubMedCrossRef Maggio M, Lauretani F, Ceda GP et al (2010) Estradiol and metabolic syndrome in older Italian men: The InCHIANTI Study. J Androl 31:155–162PubMedCrossRef
11.
go back to reference Inaba M (2004) Secondary osteoporosis: thyrotoxicosis, rheumatoid arthritis, and diabetes mellitus. J Bone Miner Metab 22:287–292PubMedCrossRef Inaba M (2004) Secondary osteoporosis: thyrotoxicosis, rheumatoid arthritis, and diabetes mellitus. J Bone Miner Metab 22:287–292PubMedCrossRef
12.
go back to reference Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392PubMedCrossRef Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392PubMedCrossRef
13.
go back to reference Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, Chihara K (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217PubMedCrossRef Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, Chihara K (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217PubMedCrossRef
14.
go back to reference Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J, Battaglia E (2004) Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int 74:136–142PubMedCrossRef Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J, Battaglia E (2004) Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int 74:136–142PubMedCrossRef
15.
go back to reference Hanley DA, Brown JP, Tenenhouse A et al (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 18:784–790PubMedCrossRef Hanley DA, Brown JP, Tenenhouse A et al (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 18:784–790PubMedCrossRef
16.
go back to reference Tsuda K, Nishio I, Masuyama Y (2001) Bone mineral density in women with essential hypertension. Am J Hypertens 14:704–707PubMedCrossRef Tsuda K, Nishio I, Masuyama Y (2001) Bone mineral density in women with essential hypertension. Am J Hypertens 14:704–707PubMedCrossRef
17.
go back to reference Gotoh M, Mizuno K, Ono Y, Takahashi M (2005) High blood pressure, bone-mineral loss and insulin resistance in women. Hypertens Res 28:565–570PubMedCrossRef Gotoh M, Mizuno K, Ono Y, Takahashi M (2005) High blood pressure, bone-mineral loss and insulin resistance in women. Hypertens Res 28:565–570PubMedCrossRef
18.
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 17:426–432PubMedCrossRef 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 17:426–432PubMedCrossRef
19.
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
20.
go back to reference Yamaguchi T, Kanazawa I, Yamamoto M, Kurioka S, Yamauchi M, Yano S, Sugimoto T (2009) Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone 45:174–179PubMedCrossRef Yamaguchi T, Kanazawa I, Yamamoto M, Kurioka S, Yamauchi M, Yano S, Sugimoto T (2009) Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone 45:174–179PubMedCrossRef
21.
go back to reference Szulc P, Kiel DP, Delmas PD (2008) Calcifications in the abdominal aorta predict fractures in men: MINOS study. J Bone Miner Res 23:95–102PubMedCrossRef Szulc P, Kiel DP, Delmas PD (2008) Calcifications in the abdominal aorta predict fractures in men: MINOS study. J Bone Miner Res 23:95–102PubMedCrossRef
22.
go back to reference Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431PubMedCrossRef Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431PubMedCrossRef
23.
go back to reference Kim JH, Choi HJ, Kim MJ, Shin CS, Cho NH (2011) Fat mass is negatively associated with bone mineral content in Koreans. Osteoporos Int 23:2009–2016PubMedCrossRef Kim JH, Choi HJ, Kim MJ, Shin CS, Cho NH (2011) Fat mass is negatively associated with bone mineral content in Koreans. Osteoporos Int 23:2009–2016PubMedCrossRef
24.
go back to reference Expert Panel on Detection E, And Treatment of High Blood Cholesterol In Adults (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285:2486–2497 Expert Panel on Detection E, And Treatment of High Blood Cholesterol In Adults (2001) Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285:2486–2497
25.
go back to reference Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062PubMedCrossRef Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062PubMedCrossRef
26.
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 92:1640–1646PubMedCrossRef Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646PubMedCrossRef
27.
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
28.
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
29.
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 144:335–345PubMedCrossRef 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 144:335–345PubMedCrossRef
30.
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
31.
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 92:4161–4164PubMedCrossRef 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 92:4161–4164PubMedCrossRef
32.
go back to reference Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10PubMed Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10PubMed
33.
go back to reference Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complicat 17:39–58PubMedCrossRef Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complicat 17:39–58PubMedCrossRef
34.
go back to reference Dennison EM, Syddall HE, Aihie Sayer A, Martin HJ, Cooper C (2007) Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort Study. QJM 100:297–303PubMedCrossRef Dennison EM, Syddall HE, Aihie Sayer A, Martin HJ, Cooper C (2007) Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort Study. QJM 100:297–303PubMedCrossRef
35.
go back to reference Bagger YZ, Rasmussen HB, Alexandersen P, Werge T, Christiansen C, Tanko LB (2007) Links between cardiovascular disease and osteoporosis in postmenopausal women: serum lipids or atherosclerosis per se? Osteoporos Int 18:505–512PubMedCrossRef Bagger YZ, Rasmussen HB, Alexandersen P, Werge T, Christiansen C, Tanko LB (2007) Links between cardiovascular disease and osteoporosis in postmenopausal women: serum lipids or atherosclerosis per se? Osteoporos Int 18:505–512PubMedCrossRef
36.
go back to reference Sivas F, Alemdaroglu E, Elverici E, Kulug T, Ozoran K (2009) Serum lipid profile: its relationship with osteoporotic vertebrae fractures and bone mineral density in Turkish postmenopausal women. Rheumatol Int 29:885–890PubMedCrossRef Sivas F, Alemdaroglu E, Elverici E, Kulug T, Ozoran K (2009) Serum lipid profile: its relationship with osteoporotic vertebrae fractures and bone mineral density in Turkish postmenopausal women. Rheumatol Int 29:885–890PubMedCrossRef
37.
go back to reference Yaturu S, Humphrey S, Landry C, Jain SK (2009) Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit 15:CR5-9 Yaturu S, Humphrey S, Landry C, Jain SK (2009) Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit 15:CR5-9
38.
go back to reference Laaksonen DE, Niskanen L, Punnonen K, Nyyssonen K, Tuomainen TP, Salonen R, Rauramaa R, Salonen JT (2003) Sex hormones, inflammation and the metabolic syndrome: a population-based study. Eur J Endocrinol 149:601–608PubMedCrossRef Laaksonen DE, Niskanen L, Punnonen K, Nyyssonen K, Tuomainen TP, Salonen R, Rauramaa R, Salonen JT (2003) Sex hormones, inflammation and the metabolic syndrome: a population-based study. Eur J Endocrinol 149:601–608PubMedCrossRef
39.
go back to reference Muller M, Grobbee DE, den Tonkelaar I, Lamberts SW, van der Schouw YT (2005) Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab 90:2618–2623PubMedCrossRef Muller M, Grobbee DE, den Tonkelaar I, Lamberts SW, van der Schouw YT (2005) Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab 90:2618–2623PubMedCrossRef
40.
go back to reference Falahati-Nini A, Riggs BL, Atkinson EJ, O’Fallon WM, Eastell R, Khosla S (2000) Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest 106:1553–1560PubMedCrossRef Falahati-Nini A, Riggs BL, Atkinson EJ, O’Fallon WM, Eastell R, Khosla S (2000) Relative contributions of testosterone and estrogen in regulating bone resorption and formation in normal elderly men. J Clin Invest 106:1553–1560PubMedCrossRef
Metadata
Title
Association between metabolic syndrome and bone mineral density in Korea: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008
Authors
Taehun Kim
Sangshin Park
Yun-Suk Pak
Sangyoon Lee
Eun-Hee Lee
Publication date
01-11-2013
Publisher
Springer Japan
Published in
Journal of Bone and Mineral Metabolism / Issue 6/2013
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-013-0459-4

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