Background: Decreased bone mineral density (BMD) has been linked to metabolic disorders, such as type 2 diabetes. However, results regarding the metabolic syndrome (MetS), a cluster of at least 3 of 5 cardiovascular risk parameters with potentially contradictory effects on BMD are still inconclusive. Objective: We investigated the effect of MetS and its single parameters on BMD at 3 sites in community-dwelling older subjects. Methods: 1,402 subjects (51.1% female, 68 ± 4 years old) from the Berlin Aging Study II (BASE-II) were included. MetS was defined as suggested by IDF/NHLBI/AHA. Insulin resistance (IR) was assessed by the homeostasis model of IR. BMD (lumbar spine, femur neck, hip) and trunk fat were measured by dual-energy X-ray absorptiometry. Osteoporosis was defined by a T score of ≤-2.5. Results: MetS was present in 29.6% of women and 41.7% of men. In regression models, we observed a positive association of MetS with the BMD of the lumbar spine (p = 0.005) and hip (p = 0.028) in women even after adjustment for risk factors, but no effect of the single parameters apart from IR. In contrast, there was no association between MetS and BMD in men. However, higher trunk fat and higher waist circumference were associated with lower levels of BMD in men with or without MetS (p < 0.05). Conclusion: We obtained different results in men and women. In women, the positive though slight effect of MetS on BMD could not be explained by single MetS components apart from IR. In men, central obesity was negatively associated with BMD, suggesting that the metabolic effects driven by visceral fat have a negative impact.

1.
Kanis JA: Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 1994;4:368-381.
2.
Choi SH, An JH, Lim S, Koo BK, Park SE, Chang HJ, et al: Lower bone mineral density is associated with higher coronary calcification and coronary plaque burdens by multidetector row coronary computed tomography in pre- and postmenopausal women. Clin Endocrinol 2009;71:644-651.
3.
Sumino H, Ichikawa S, Kasama S, Takahashi T, Kumakura H, Takayama Y, et al: Elevated arterial stiffness in postmenopausal women with osteoporosis. Maturitas 2006;55:212-218.
4.
Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR: Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 2005;20:1912-1920.
5.
Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, et al: Diagnosis and management of the metabolic syndrome an American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Circulation 2005;112:2735-2752.
6.
Alberti K, Zimmet P, Shaw J: Metabolic syndrome - a new world-wide definition. A consensus statement from the international diabetes federation. Diabet Med 2006;23:469-480.
7.
Gami AS, Witt BJ, Howard DE, Erwin PJ, Gami LA, Somers VK, et al: Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol 2007;49:403-414.
8.
Alberti K, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al: Harmonizing the Metabolic Syndrome, A Joint Interim Statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 2009;120:1640-1645.
9.
Kinjo M, Setoguchi S, Solomon DH: Bone mineral density in adults with the metabolic syndrome: analysis in a population-based U.S. sample. J Clin Endocrinol Metab 2007;92:4161-4164.
10.
Kim HY, Choe JW, Kim HK, Bae SJ, Kim BJ, Lee SH, et al: Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif Tissue Int 2010;86:350-358.
11.
von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E: Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int 2007;18:1337-1344.
12.
Szulc P, Varennes A, Delmas PD, Goudable J, Chapurlat R: Men with metabolic syndrome have lower bone mineral density but lower fracture risk - the MINOS study. J Bone Miner Res 2010;25:1446-1454.
13.
Hwang DK, Choi HJ: The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 2010;21:425-431.
14.
Xue P, Gao P, Li Y: The association between metabolic syndrome and bone mineral density: a meta-analysis. Endocrine 2012;42:546-554.
15.
Zhou J, Zhang Q, Yuan X, Wang J, Li C, Sheng H, et al: Association between metabolic syndrome and osteoporosis: a meta-analysis. Bone 2013;57:30-35.
16.
Maggio M, Lauretani F, Ceda GP, Bandinelli S, Basaria S, Paolisso G, et al: Estradiol and metabolic syndrome in older Italian men: The InCHIANTI Study. J Androl 2010;31:155-162.
17.
Nelson LR, Bulun SE: Estrogen production and action. J Am Acad Dermatol 2001;45:S116-S124.
18.
Dupuy A-M, Jaussent I, Lacroux A, Durant R, Cristol J-P, Delcourt C: Waist circumference adds to the variance in plasma C-reactive protein levels in elderly patients with metabolic syndrome. Gerontology 2007;53:329-339.
19.
Barbour KE, Zmuda JM, Boudreau R, Strotmeyer ES, Horwitz MJ, Evans RW, et al: Adipokines and the risk of fracture in older adults. J Bone Miner Res 2011;26:1568-1576.
20.
Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, et al: Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 2008;23:17-29.
21.
Eren E, Ellidag HY, Aydin O, Yılmaz N: HDL-associated paraoxonase 1 as a bridge between postmenopausal osteoporosis and cardiovascular disease. Chonnam Med J 2014;50:75-81.
22.
D'Amelio P, Di Bella S, Tamone C, Ravazzoli MG, Cristofaro MA, Di Stefano M, et al: HDL cholesterol and bone mineral density in normal-weight postmenopausal women: is there any possible association? Panminerva Med 2008;50:89-96.
23.
Dennison EM, Syddall HE, Sayer AA, Martin HJ, Cooper C; the Hertfordshire Cohort Study Group: Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort Study. QJM 2007;100:297-303.
24.
Bagger YZ, Rasmussen HB, Alexandersen P, Werge T, Christiansen C, Tanko LB: Links between cardiovascular disease and osteoporosis in postmenopausal women: serum lipids or atherosclerosis per se? Osteoporosis Int 2007;18:505-512.
25.
Cappuccio FP, Meilahn E, Zmuda JM, Cauley JA: High blood pressure and bone-mineral loss in elderly white women: a prospective study. Study of Osteoporotic Fractures Research Group. Lancet 1999;354:971-975.
26.
Bertram L, Bockenhoff A, Demuth I, Duzel S, Eckardt R, Li SC, et al: Cohort profile: The Berlin Aging Study II (BASE-II). Int J Epidemiol 2014;43:703-712.
27.
Barrett-Connor E, Kritz-Silverstein D: Does hyperinsulinemia preserve bone? Diabetes Care 1996;19:1388-1392.
28.
Stolk R, Van Daele P, Pols H, Burger H, Hofman A, Birkenhäger J, et al: Hyperinsulinemia and bone mineral density in an elderly population: The Rotterdam Study. Bone 1996;18:545-549.
29.
Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T: Bone mineral density measured by dual energy x-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone 1993;14:29-33.
30.
Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, Cooper C: Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia 2004;47:1963-1968.
31.
Barrett-Connor E, Holbrook TL: Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 1992;268:3333-3337.
32.
Hernández JL, Olmos JM, Pariente E, Martínez J, Valero C, García-Velasco P, et al: Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 2010;17:955-961.
33.
Jeon YK, Lee JG, Kim SS, Kim BH, Kim S-J, Kim YK, et al: Association between bone mineral density and metabolic syndrome in pre-and postmenopausal women. Endocr J 2010;58:87-93.
34.
Yoldemir T, Erenus M: The impact of metabolic syndrome on bone mineral density in postmenopausal women. Gynecol Endocrinol 2012;28:391-395.
35.
Kuk JL, Lee S, Heymsfield SB, Ross R: Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 2005;81:1330-1334.
36.
Kim T, Park S, Pak YS, Lee S, Lee EH: Association between metabolic syndrome and bone mineral density in Korea: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV), 2008. J Bone Miner Metab 2013;31:652-662.
37.
Janssen I, Heymsfield SB, Allison DB, Kotler DP, Ross R: Body mass index and waist circumference independently contribute to the prediction of nonabdominal, abdominal subcutaneous, and visceral fat. Am J Clin Nutr 2002;75:683-688.
38.
Lemieux S, Prud'homme D, Bouchard C, Tremblay A, Després J-P: Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 1993;58:463-467.
39.
Kotani K, Tokunaga K, Fujioka S, Kobatake T, Keno Y, Yoshida S, et al: Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes Relat Metab Disord 1994;18:207-202.
40.
Hung J, McQuillan BM, Chapman CM, Thompson PL, Beilby JP: Elevated interleukin-18 levels are associated with the metabolic syndrome independent of obesity and insulin resistance. Arterioscler Thromb Vasc Biol 2005;25:1268-1273.
41.
Wajchenberg BL: Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000;21:697-738.
42.
Peeke PM, Chrousos GP: Hypercortisolism and obesity. Ann NY Acad Sci 1995;771:665-676.
43.
Chiodini I, Tauchmanovà L, Torlontano M, Battista C, Guglielmi G, Cammisa M, et al: Bone involvement in eugonadal male patients with adrenal incidentaloma and subclinical hypercortisolism. J Clin Endocrinol Metab 2002;87:5491-5494.
44.
Migliaccio S, Greco EA, Fornari R, Donini LM, Lenzi A: Is obesity in women protective against osteoporosis? Diabetes Metab Syndr Obes 2011;4:273.
45.
Reid IR: Relationships among body mass, its components, and bone. Bone 2002;31:547-555.
46.
Muller M, Grobbee DE, den Tonkelaar I, Lamberts SW, van der Schouw YT: Endogenous sex hormones and metabolic syndrome in aging men. J Clin Endocrinol Metab 2005;90:2618-2623.
47.
Migliaccio S, Francomano D, Bruzziches R, Greco EA, Fornari R, Donini LM, et al: Trunk fat negatively influences skeletal and testicular functions in obese men: clinical implications for the aging male. Int J Endocrinol 2013;182753:20.
48.
Tintut Y, Morony S, Demer LL: Hyperlipidemia promotes osteoclastic potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol 2004;24:e6-e10.
49.
Ford ES, Giles WH, Dietz WH: Prevalence of the metabolic syndrome among us adults: findings from the third national health and nutrition examination survey. JAMA 2002;287:356-359.
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