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Erschienen in: Osteoporosis International 8/2013

01.08.2013 | Original Article

Association between metabolic syndrome and bone loss at various skeletal sites in postmenopausal women: a 3-year retrospective longitudinal study

verfasst von: B.-J. Kim, S. H. Ahn, S. J. Bae, E. H. Kim, T.-H. Kim, S. H. Lee, H.-K. Kim, J. W. Choe, S.-Y. Kim, J.-M. Koh, G. S. Kim

Erschienen in: Osteoporosis International | Ausgabe 8/2013

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Abstract

Summary

Although the presence of metabolic syndrome (MetS) and increasing numbers of MetS components were associated with attenuated bone loss at various skeletal sites in postmenopausal women, this beneficial effect of MetS on bone mass can be mainly explained by higher mechanical loading in the affected subjects.

Introduction

Previous cross-sectional epidemiological studies reported the inconsistent results regarding the combined effects of MetS on bone mass. In our present report, we performed a large, longitudinal study to evaluate MetS in relation to annualized bone mineral density (BMD) changes in postmenopausal Korean women.

Methods

The study cohort consisted of 1,218 postmenopausal women who had undergone comprehensive routine health examinations with an average follow-up interval of 3 years. The BMD at the lumbar spine and proximal femur sites was measured with dual-energy X-ray absorptiometry using the same equipment at baseline and at follow-up.

Results

Following adjustment for age, baseline BMD, and lifestyle factors, the women with MetS had 21.7, 17.0, 26.7, and 31.1 % less bone loss at the total femur, femur neck, trochanter, and lumbar spine, respectively, compared with MetS-free women (P = 0.004 to 0.041). Consistently, the rates of bone loss at all skeletal sites were linearly attenuated with increasing numbers of MetS components (P = 0.004 to <0.001). Importantly, when weight and height were added as confounding factors, the differences and trends of annualized BMD changes according to the MetS status disappeared.

Conclusion

Our current results indicate that the beneficial effects of MetS on bone mass can be mainly explained by higher mechanical loading in the affected subjects. Consequently, MetS per se may not be a meaningful concept for predicting future bone loss and for explaining associations between osteoporosis and cardiovascular diseases.
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Literatur
1.
Zurück zum Zitat Kado DM, Browner WS, Blackwell T, Gore R, Cummings SR (2000) Rate of bone loss is associated with mortality in older women: a prospective study. J Bone Miner Res 15:1974–1980PubMedCrossRef Kado DM, Browner WS, Blackwell T, Gore R, Cummings SR (2000) Rate of bone loss is associated with mortality in older women: a prospective study. J Bone Miner Res 15:1974–1980PubMedCrossRef
2.
Zurück zum Zitat von der Recke P, Hansen MA, Hassager C (1999) The association between low bone mass at the menopause and cardiovascular mortality. Am J Med 106:273–278PubMedCrossRef von der Recke P, Hansen MA, Hassager C (1999) The association between low bone mass at the menopause and cardiovascular mortality. Am J Med 106:273–278PubMedCrossRef
3.
Zurück zum Zitat 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
4.
Zurück zum Zitat 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.
Zurück zum Zitat 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.
Zurück zum Zitat Koh JM, Khang YH, Jung CH, Bae S, Kim DJ, Chung YE, Kim GS (2005) Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int 16:1263–1271PubMedCrossRef Koh JM, Khang YH, Jung CH, Bae S, Kim DJ, Chung YE, Kim GS (2005) Higher circulating hsCRP levels are associated with lower bone mineral density in healthy pre- and postmenopausal women: evidence for a link between systemic inflammation and osteoporosis. Osteoporos Int 16:1263–1271PubMedCrossRef
7.
Zurück zum Zitat 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.
Zurück zum Zitat 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 288:2709–2716PubMedCrossRef 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 288:2709–2716PubMedCrossRef
9.
Zurück zum Zitat Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M, Taskinen MR, Groop L (2001) Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24:683–689PubMedCrossRef Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M, Taskinen MR, Groop L (2001) Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24:683–689PubMedCrossRef
10.
Zurück zum Zitat 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
11.
Zurück zum Zitat 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
12.
Zurück zum Zitat Hernandez JL, Olmos JM, Pariente E, Martinez J, Valero C, Garcia-Velasco P, Nan D, Llorca J, Gonzalez-Macias J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17:955–961PubMedCrossRef Hernandez JL, Olmos JM, Pariente E, Martinez J, Valero C, Garcia-Velasco P, Nan D, Llorca J, Gonzalez-Macias J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17:955–961PubMedCrossRef
13.
Zurück zum Zitat 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
14.
Zurück zum Zitat 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
15.
Zurück zum Zitat Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD, McClung M, Hosking D, Yates AJ, Christiansen C (1999) Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. Early Postmenopausal Intervention Cohort (EPIC) study group. J Bone Miner Res 14:1622–1627PubMedCrossRef Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD, McClung M, Hosking D, Yates AJ, Christiansen C (1999) Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. Early Postmenopausal Intervention Cohort (EPIC) study group. J Bone Miner Res 14:1622–1627PubMedCrossRef
16.
Zurück zum Zitat Smith BJ, Lerner MR, Bu SY, Lucas EA, Hanas JS, Lightfoot SA, Postier RG, Bronze MS, Brackett DJ (2006) Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone 38:378–386PubMedCrossRef Smith BJ, Lerner MR, Bu SY, Lucas EA, Hanas JS, Lightfoot SA, Postier RG, Bronze MS, Brackett DJ (2006) Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone 38:378–386PubMedCrossRef
17.
Zurück zum Zitat Kim BJ, Yu YM, Kim EN, Chung YE, Koh JM, Kim GS (2007) Relationship between serum hsCRP concentration and biochemical bone turnover markers in healthy pre- and postmenopausal women. Clin Endocrinol (Oxf) 67:152–158CrossRef Kim BJ, Yu YM, Kim EN, Chung YE, Koh JM, Kim GS (2007) Relationship between serum hsCRP concentration and biochemical bone turnover markers in healthy pre- and postmenopausal women. Clin Endocrinol (Oxf) 67:152–158CrossRef
18.
Zurück zum Zitat 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
19.
Zurück zum Zitat Ahmed LA, Schirmer H, Berntsen GK, Fønnebø V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromsø study. Osteoporos Int 17:426–432PubMedCrossRef Ahmed LA, Schirmer H, Berntsen GK, Fønnebø V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromsø study. Osteoporos Int 17:426–432PubMedCrossRef
20.
Zurück zum Zitat 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 8:567–573PubMedCrossRef 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 8:567–573PubMedCrossRef
21.
Zurück zum Zitat Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169PubMed Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169PubMed
22.
Zurück zum Zitat Stolk RP, Van Daele PL, Pols HA, Burger H, Hofman A, Birkenhager JC, Lamberts SW, Grobbee DE (1996) Hyperinsulinemia and bone mineral density in an elderly population: the Rotterdam Study. Bone 18:545–549PubMedCrossRef Stolk RP, Van Daele PL, Pols HA, Burger H, Hofman A, Birkenhager JC, Lamberts SW, Grobbee DE (1996) Hyperinsulinemia and bone mineral density in an elderly population: the Rotterdam Study. Bone 18:545–549PubMedCrossRef
23.
24.
Zurück zum Zitat Ohta H, Ikeda T, Masuzawa T, Makita K, Suda Y, Nozawa S (1993) Differences in axial bone mineral density, serum levels of sex steroids, and bone metabolism between postmenopausal and age- and body size-matched premenopausal subjects. Bone 14:111–116PubMedCrossRef Ohta H, Ikeda T, Masuzawa T, Makita K, Suda Y, Nozawa S (1993) Differences in axial bone mineral density, serum levels of sex steroids, and bone metabolism between postmenopausal and age- and body size-matched premenopausal subjects. Bone 14:111–116PubMedCrossRef
25.
Zurück zum Zitat Reid I, Richards JB (2009) Adipokine effects on bone. Clin Rev Bone Miner Metab 7:240–248CrossRef Reid I, Richards JB (2009) Adipokine effects on bone. Clin Rev Bone Miner Metab 7:240–248CrossRef
26.
Zurück zum Zitat Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, Cortet B (2011) Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. J Clin Endocrinol Metab 96:2703–2713PubMedCrossRef Biver E, Salliot C, Combescure C, Gossec L, Hardouin P, Legroux-Gerot I, Cortet B (2011) Influence of adipokines and ghrelin on bone mineral density and fracture risk: a systematic review and meta-analysis. J Clin Endocrinol Metab 96:2703–2713PubMedCrossRef
27.
Zurück zum Zitat Yatagai T, Nagasaka S, Taniguchi A, Fukushima M, Nakamura T, Kuroe A, Nakai Y, Ishibashi S (2003) Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism 52:1274–1278PubMedCrossRef Yatagai T, Nagasaka S, Taniguchi A, Fukushima M, Nakamura T, Kuroe A, Nakai Y, Ishibashi S (2003) Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism 52:1274–1278PubMedCrossRef
28.
Zurück zum Zitat Nakashima R, Kamei N, Yamane K, Nakanishi S, Nakashima A, Kohno N (2006) Decreased total and high molecular weight adiponectin are independent risk factors for the development of type 2 diabetes in Japanese-Americans. J Clin Endocrinol Metab 91:3873–3877PubMedCrossRef Nakashima R, Kamei N, Yamane K, Nakanishi S, Nakashima A, Kohno N (2006) Decreased total and high molecular weight adiponectin are independent risk factors for the development of type 2 diabetes in Japanese-Americans. J Clin Endocrinol Metab 91:3873–3877PubMedCrossRef
29.
Zurück zum Zitat Badman MK, Flier JS (2007) The adipocyte as an active participant in energy balance and metabolism. Gastroenterology 132:2103–2115PubMedCrossRef Badman MK, Flier JS (2007) The adipocyte as an active participant in energy balance and metabolism. Gastroenterology 132:2103–2115PubMedCrossRef
30.
Zurück zum Zitat 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
31.
Zurück zum Zitat Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949PubMedCrossRef Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949PubMedCrossRef
32.
Zurück zum Zitat Gabay C, Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340:448–454PubMedCrossRef Gabay C, Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340:448–454PubMedCrossRef
33.
Zurück zum Zitat 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
34.
Zurück zum Zitat 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
35.
Zurück zum Zitat Xu S, Yu JJ (2006) Beneath the minerals, a layer of round lipid particles was identified to mediate collagen calcification in compact bone formation. Biophys J 91:4221–4229PubMedCrossRef Xu S, Yu JJ (2006) Beneath the minerals, a layer of round lipid particles was identified to mediate collagen calcification in compact bone formation. Biophys J 91:4221–4229PubMedCrossRef
36.
Zurück zum Zitat 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 Miner Res 25:1446–1454PubMedCrossRef 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 Miner Res 25:1446–1454PubMedCrossRef
37.
Zurück zum Zitat Green S, Anstiss CL, Fishman WH (1971) Automated differential isoenzyme analysis. II. The fractionation of serum alkaline phosphatases into “liver”, “intestinal” and “other” components. Enzymologia 41:9–26PubMed Green S, Anstiss CL, Fishman WH (1971) Automated differential isoenzyme analysis. II. The fractionation of serum alkaline phosphatases into “liver”, “intestinal” and “other” components. Enzymologia 41:9–26PubMed
38.
Zurück zum Zitat van Straalen JP, Sanders E, Prummel MF, Sanders GT (1991) Bone-alkaline phosphatase as indicator of bone formation. Clin Chim Acta 201:27–33PubMedCrossRef van Straalen JP, Sanders E, Prummel MF, Sanders GT (1991) Bone-alkaline phosphatase as indicator of bone formation. Clin Chim Acta 201:27–33PubMedCrossRef
Metadaten
Titel
Association between metabolic syndrome and bone loss at various skeletal sites in postmenopausal women: a 3-year retrospective longitudinal study
verfasst von
B.-J. Kim
S. H. Ahn
S. J. Bae
E. H. Kim
T.-H. Kim
S. H. Lee
H.-K. Kim
J. W. Choe
S.-Y. Kim
J.-M. Koh
G. S. Kim
Publikationsdatum
01.08.2013
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 8/2013
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-013-2292-y

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