Abstract
Summary
We examined the relationships between bone mineral density (BMD) and metabolic syndrome in 6,659 men and 7,826 women from South Korean. After adjusting for age, body mass index (BMI), tobacco and alcohol use, and regular exercise, low BMD is especially associated with metabolic syndrome in South Korean men.
Purpose
This study examined the relationships between BMD and metabolic syndrome (MS) in South Korean adults.
Methods
A total of 14,485 adults (6,659 men and 7,826 women) in the Korea National Health and Nutrition Examination Survey conducted from 2008 to 2010 were analyzed. We used multivariable regression models to examine the relationship between low BMD and MS. We calculated homeostasis model assessment and insulin resistance (HOMA-IR). MS was defined according to AHA/NHLBI criteria for Asians. BMD was measured at the lumbar spine (LS), femur neck (FN), total hip (TH), trochanter, and intertrochanter.
Results
After adjustment for age, BMI, tobacco and alcohol use, and regular exercise, the TH and FN BMD were significantly lower in men with MS than in men without MS (p < 0.05). However, there were no differences in premenopausal and postmenopausal women. In men, BMD was positively correlated with BMI, and high density lipoprotein cholesterol, but was negatively correlated with insulin, HOMA-IR, and triglyceride at all three sites (p < 0.05). Along with an increase of BMD (0.1 g/cm2), the odds ratios (ORs) for obesity and abdominal obesity were all greater than 1 at all sites in both genders. The ORs for hypertension and MS were 0.937 (0.879–0.998) and 0.899 (0.840–0.962), respectively at FN, and the OR for diabetes mellitus was 1.103 (1.017–1.196) at LS in men. In postmenopausal women, the OR for hypertension was 1.133 (1.029–1.246) at LS.
Conclusions
Low BMD was especially associated with MS in South Korean men.
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References
Braithwaite RS, Col NF, Wong JB (2003) Estimating hip fracture morbidity, mortality and costs. J Am Geriatr Soc 51(3):364–370
Van Der Klift M, Pols HA, Geleijnse JM, Van Der Kuip DA, Hofman A, De Laet CE (2002) Bone mineral density and mortality in elderly men and women: the Rotterdam Study. Bone 30(4):643–648
Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Roger VL, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J, American Heart Association Statistics C, Stroke Statistics S (2010) Heart disease and stroke statistics–2010 update: a report from the American Heart Association. Circulation 121(7):e46–e215. doi:10.1161/circulationaha.109.192667
Browner WS, Pressman AR, Nevitt MC, Cauley JA, Cummings SR (1993) Association between low bone density and stroke in elderly women. The study of osteoporotic fractures. Stroke; a J of Cerebral Circulation 24(7):940–946
Mussolino ME, Gillum RF (2006) Bone mineral density and hypertension prevalence in postmenopausal women: results from the Third National Health and Nutrition Examination Survey. Ann Epidemiol 16(5):395–399. doi:10.1016/j.annepidem.2005.06.051
Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone and Mineral Res: The Official J of the Am Soc for Bone and Mineral Res 20(11):1912–1920. doi:10.1359/jbmr.050711
Jørgensen L, Engstad T, Jacobsen BK (2001) Bone mineral density in acute stroke patients: low bone mineral density may predict first stroke in women. Stroke; a J of Cerebral Circulation 32(1):47–51
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(6):589–595
Expert Panel on Detection E, Treatment of High Blood Cholesterol in A (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(19):2486–2497
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, American Heart A, National Heart L, Blood I (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112(17):2735–2752. doi:10.1161/circulationaha.105.169404
Rana JS, Nieuwdorp M, Jukema JW, Kastelein JJ (2007) Cardiovascular metabolic syndrome—an interplay of, obesity, inflammation, diabetes and coronary heart disease. Diabetes, obesity & metabolism 9(3):218–232. doi:10.1111/j.1463-1326.2006.00594.x
National Cholesterol Education Program Expert Panel on Detection E, Treatment of High Blood Cholesterol in A (2002) 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) final report. Circulation 106(25):3143–3421
Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT (2002) The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288(21):2709–2716
Ministry of Health and Welfare, Korea Centers for Disease Control and Prevention (2006) The Third Korea National Health and Nutrition Examination Survey (KNHANES III), 2005: Health Examination. Korea Centers for Disease Control and Prevention, Seoul
Hernández JL, Olmos JM, Pariente E, Martínez J, Valero C, García-Velasco P, Nan D, Llorca J, González-Macías J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause (New York, NY) 17(5):955–961. doi:10.1097/gme.0b013e3181e39a15
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(11):4161–4164. doi:10.1210/jc.2007-0757
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. Osteoporosis Int 18(10):1337–1344. doi:10.1007/s00198-007-0385-1
Kim HY, Choe JW, Kim HK, Bae SJ, Kim BJ, Lee SH, Koh JM, Han KO, Park HM, Kim GS (2010) Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif Tissue Int 86(5):350–358. doi:10.1007/s00223-010-9347-2
Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporosis Int 21(3):425–431. doi:10.1007/s00198-009-0990-2
Hagströmer M, Oja P, Sjöström M (2006) The International Physical Activity Questionnaire (IPAQ): a study of concurrent and construct validity. Public Health Nutrition 9(6):755–762
Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28(7):412–419
Sakkinen PA, Wahl P, Cushman M, Lewis MR, Tracy RP (2000) Clustering of procoagulation, inflammation, and fibrinolysis variables with metabolic factors in insulin resistance syndrome. Am J Epidemiol 152(10):897–907
Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2(1):35–43. doi:10.1038/ncprheum0070
Lazarenko OP, Rzonca SO, Hogue WR, Swain FL, Suva LJ, Lecka-Czernik B (2007) Rosiglitazone induces decreases in bone mass and strength that are reminiscent of aged bone. Endocrinology 148(6):2669–2680. doi:10.1210/en.2006-1587
Beck TJ, Petit MA, Wu G, LeBoff MS, Cauley JA, Chen Z (2009) Does obesity really make the femur stronger? BMD, geometry, and fracture incidence in the women’s health initiative-observational study. J Bone and Mineral Res 24(8):1369–1379. doi:10.1359/jbmr.090307
Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R (2010) Men with metabolic syndrome have lower bone mineral density but lower fracture risk—the MINOS study. J Bone and Mineral Res 25(6):1446–1454. doi:10.1002/jbmr.13
Rasouli N, Kern PA (2008) Adipocytokines and the metabolic complications of obesity. J Clin Endocrinol Metab 93(11 Suppl 1):S64–S73. doi:10.1210/jc.2008-1613
Wellen KE, Hotamisligil GS (2003) Obesity-induced inflammatory changes in adipose tissue. J Clin Invest 112(12):1785–1788. doi:10.1172/jci20514
Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone and Mineral Res 17(9):1563–1569. doi:10.1359/jbmr.2002.17.9.1563
Ağbaht K, Gürlek A, Karakaya J, Bayraktar M (2009) Circulating adiponectin represents a biomarker of the association between adiposity and bone mineral density. Endocrine 35(3):371–379. doi:10.1007/s12020-009-9158-2
Barbour KE, Zmuda JM, Boudreau R, Strotmeyer ES, Horwitz MJ, Evans RW, Kanaya AM, Harris TB, Cauley JA (2012) The effects of adiponectin and leptin on changes in bone mineral density. Osteoporosis Int 23(6):1699–1710. doi:10.1007/s00198-011-1768-x
Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. South African Med J = Suid-Afrikaanse tydskrif vir geneeskunde 86(9):1081–1084
Saarelainen J, Honkanen R, Kroger H, Tuppurainen M, Jurvelin JS, Niskanen L (2011) Body fat distribution is associated with lumbar spine bone density independently of body weight in postmenopausal women. Maturitas 69(1):86–90. doi:10.1016/j.maturitas.2011.02.009
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(6):1330–1334
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 of Epidemiol 144(4):335–345
Kang SM, Yoon JW, Ahn HY, Kim SY, Lee KH, Shin H, Choi SH, Park KS, Jang HC, Lim S (2011) Android fat depot is more closely associated with metabolic syndrome than abdominal visceral fat in elderly people. PLoS One 6(11):e27694. doi:10.1371/journal.pone.0027694
Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complications 17(1):39–58
Jankowska EA, Rogucka E, Medraś 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(6):384–389
Ljung T, Holm G, Friberg P, Andersson B, Bengtsson BA, Svensson J, Dallman M, McEwen B, Björntorp P (2000) The activity of the hypothalamic-pituitary-adrenal axis and the sympathetic nervous system in relation to waist/hip circumference ratio in men. Obes Res 8(7):487–495. doi:10.1038/oby.2000.61
Rosmond R, Björntorp P (2000) Low cortisol production in chronic stress. The connection stress-somatic disease is a challenge for future research. Lakartidningen 97(38):4120–4124
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(5):2618–2623. doi:10.1210/jc.2004-1158
Brownbill RA, Ilich JZ (2006) Lipid profile and bone paradox: higher serum lipids are associated with higher bone mineral density in postmenopausal women. J Women’s Health 15(3):261–270. doi:10.1089/jwh.2006.15.261
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(2):136–142. doi:10.1007/s00223-003-0050-4
Sivas F, Alemdaroğlu E, Elverici E, Kuluğ T, 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(8):885–890. doi:10.1007/s00296-008-0784-4
Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, Berliner JA, Demer LL (1997) Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation. A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol 17(4):680–687
Acknowledgments
The authors thank the Korea Centers for Disease Control and Prevention, who performed the KNHANES. Thanks to Anna Kim for translating this manuscript into English.
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Kim, YH., Cho, KH., Choi, Y.S. et al. Low bone mineral density is associated with metabolic syndrome in South Korean men but not in women: The 2008–2010 Korean National Health and Nutrition Examination Survey. Arch Osteoporos 8, 142 (2013). https://doi.org/10.1007/s11657-013-0142-3
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DOI: https://doi.org/10.1007/s11657-013-0142-3