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Journal of Bone and Mineral Metabolism

, Volume 36, Issue 2, pp 200–208 | Cite as

Association between metabolic syndrome and bone mineral density in a Taiwanese elderly population

  • Song-Seng LokeEmail author
  • Hsueh-Wen Chang
  • Wen-Cheng Li
Original Article

Abstract

Previous studies have demonstrated uncertainty regarding the effect of metabolic syndrome (MetS) on bone. In the present work, we investigated the association between MetS, its components, and decreased bone mineral density (BMD) in a cross-sectional study of patients who underwent BMD measurement by dual-energy X-ray absorptiometry during a health examination. Decreased BMD was defined as either osteopenia or osteoporosis. MetS components and body mass index (BMI) were compared between individuals with normal and decreased BMD, and simple and multivariate logistic regression analyses were used to evaluate the association between the variables and decreased BMD in women and men. Among 1162 subjects in the study, the mean age was 59.9 ± 7.3 years, and 59.5% were men. The prevalence of MetS and osteoporosis was 34.2 and 19.6%, respectively. MetS was positively associated with BMD in men, while in women it was negatively associated with BMD. Regarding the relationship between MetS components and BMD, we found that in women, waist circumference (WC) and systolic and diastolic blood pressure were negatively associated with BMD, while high-density lipoprotein cholesterol (HDL-C) was positively associated. In men, WC and fasting glucose were positively associated with BMD, while HDL-C was negatively associated. We also found that an increase in the number of MetS components resulted in a significantly increased positive association with BMD, both before and after adjusting for age, in men but not in women, revealing a gender difference in the correlation between MetS components and BMD.

Keywords

Metabolic syndrome Bone mineral density Metabolic components Osteoporosis Dual-energy X-ray absorptiometry 

Notes

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interest.

References

  1. 1.
    Johnell O, Kamis JA (2006) An estimated of worldwide prevalence and disability associated with osteoporosis fractures. Osteoporosis Int 17:1726–1733CrossRefGoogle Scholar
  2. 2.
    Fink HA, Ewing SK, Ensrud KE, Barrett-Connor E, Taylor BC, Cauley JA et al (2006) Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men. J Clin Endocrinol Metab 91:3908–3915CrossRefGoogle Scholar
  3. 3.
    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 93:1952–1958CrossRefGoogle Scholar
  4. 4.
    Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK et al (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297CrossRefGoogle Scholar
  5. 5.
    Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431CrossRefGoogle Scholar
  6. 6.
    Park KK, Kim SJ, Moon ES (2010) Association between bone mineral density and metabolic syndrome in postmenopausal Korean women. Gynecol Obstet Invest 69:145–152CrossRefGoogle Scholar
  7. 7.
    Jia WP, Xiang KS, Chen L, Lu JX, Wu YM (2002) Epidemiological study on obesity and its comorbidities in urban Chinese older than 20 years of age in Shanghai, China. Obes Rev 3:157–165CrossRefGoogle Scholar
  8. 8.
    Gill TP (2001) Cardiovascular risk in the Asia-Pacific region from a nutrition and metabolic point of view: abdominal obesity. Asia Pac J Clin Nutr 10:85–89CrossRefGoogle Scholar
  9. 9.
    Wang TD, Chen WJ, Chien KL, Seh-Yi Su SS, Hsu HC, Chen MF, Liau CS, Lee YT (2001) Efficacy of cholesterol levels and ratios in predicting future coronary heart disease in a Chinese population. Am J Cardiol 88:737–743CrossRefGoogle Scholar
  10. 10.
    Chuang SY, Chen CH, Chou P (2004) Prevalence of metabolic syndrome in a large health check-up population in Taiwan. J. Chin. Med. Assoc. 67:611–620PubMedGoogle Scholar
  11. 11.
    Yang TS, Chen YR, Chen YJ, Chang CY, Ng HT (2004) Osteoporosis: prevalence in Taiwanese women. Osteoporos Int 15:345–347CrossRefGoogle Scholar
  12. 12.
    Zhou Jiaojiao, Zhang Qiang, Yuan Xiaolan, Wang Jijiao, Li Chunyan, Sheng Hui, Shen Qu, Li Hong (2013) Association between metabolic syndrome and osteoporosis: a meta-analysis. Bone 57:30–35CrossRefGoogle Scholar
  13. 13.
    Xue P, Gao P, Li YK (2012) The association between metabolic syndrome and bone mineral density: a meta-analysis. Endocrine 42:546–554CrossRefGoogle Scholar
  14. 14.
    Tseng Yao-Hsien, Huang Kui-Chou, Liu Mann-Li, Shu Wei-Tzu, Sheu Wayne Huey-Herng (2009) Association between metabolic syndrome and bone mineral loss: a cross-sectional study in Puli Township in Taiwan. Arch Gerontol Geriatr 49:S37–S40CrossRefGoogle Scholar
  15. 15.
    Ersoy B, Gökşen D, Darcan S, Mavi E, Oztürk C (1999) Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66:375–379CrossRefGoogle Scholar
  16. 16.
    Hough FS (1987) Alterations of bone and mineral metabolism in diabetes mellitus. Part II. Clinical studies in 206 patients with type I diabetes mellitus. S Afr Med J 72:120–126PubMedGoogle Scholar
  17. 17.
    Forst T, Pfützner A, Kann P, Schehler B, Lobmann R, Schäfer H, Andreas J, Bockisch A, Beyer J (1995) Peripheral osteopenia in adult patients with insulin dependent diabetes mellitus. Diabet Med 12:874–879CrossRefGoogle Scholar
  18. 18.
    Kao WH, Kammerer CM, Schneider JL, Bauer RL, Mitchell BD (2003) Type 2 diabetes is associated with increased bone mineral density in Mexican–American women. Arch Med Res 34:399–406CrossRefGoogle Scholar
  19. 19.
    Schwartz AV, Sellmeyer DE, Strotmeyer ES, Tylavsky FA, Feingold KR, Resnick HE, Shorr RI, Nevitt MC, Black DM, Cauley JA, Cummings SR, Harris TB (2005) Health ABC Study. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596–603CrossRefGoogle Scholar
  20. 20.
    Muka T, Trajanoska K, Kiefte-de Jong JC, Oei L, Uitterlinden AG, Hofman A et al (2015) The association between metabolic syndrome, bone mineral density, hip bone geometry and fracture risk: the Rotterdam study. PLoS One 10:e0129116. doi: 10.1371/journal.pone.0129116 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Esposito K, Chiodini P, Capuano A, Colao A, Guigliano D (2013) Fracture risk and bone mineral density in metabolic syndrome: a meta-analysis. J Clin Endocrinol Metab 98:3306–3314CrossRefGoogle Scholar
  22. 22.
    Yang L, Lv X, Wei D, Yue F, Guo J, Zhang T (2016) Metabolic syndrome and the risk of bone fractures: a meta-analysis of prospective cohort studies. Bone 84:52–56CrossRefGoogle Scholar
  23. 23.
    Oz SG, Guven GS, Kilicarslan A, Calik N, Beyazit Y, Sozen T (2006) Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus. J Natl Med Assoc 98:1598–1604PubMedPubMedCentralGoogle Scholar
  24. 24.
    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 33:384–389CrossRefGoogle Scholar
  25. 25.
    Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084PubMedGoogle Scholar
  26. 26.
    Torti C, Mazziotti G, Soldini PA, Focà E, Maroldi R, Gotti D, Carosi G, Giustina A (2001) High prevalence of radiological vertebral fractures in HIV-infected males. Endocrine 41:512–517CrossRefGoogle Scholar
  27. 27.
    Moon SS, Lee YS, Kim SW (2012) Association of nonalcoholic fatty liver disease with low bone mass in postmenopausal women. Endocrine 42:423–429CrossRefGoogle Scholar
  28. 28.
    Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169CrossRefGoogle Scholar
  29. 29.
    Agbaht K, Gurlek A, Karakaya J, Bayraktar M (2009) Circulating adiponectin represents a biomarker of the association between adiposity and bone mineral density. Endocrine 35:371–379CrossRefGoogle Scholar
  30. 30.
    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 8:567–573CrossRefGoogle Scholar
  31. 31.
    Marcus R, Greendale G, Blunt BA, Bush TL, Sherman S, Sherwin R, Wahner H, Wells B (1994) Correlates of bone mineral density in the postmenopausal estrogen/progestin interventions trial. J Bone Miner Res 9:1467–1476CrossRefGoogle Scholar
  32. 32.
    De Laet C, Kanis JA, Odén A, Johanson H, Johnell O, Delmas P, Eisman JA, Kroger H, Fujiwara S, Garnero P, McCloskey EV, Mellstrom D, Melton LJ 3rd, Meunier PJ, Pols HA, Reeve J, Silman A, Tenenhouse A (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338CrossRefGoogle Scholar
  33. 33.
    Gimble JM, Nuttall ME (2004) Bone and fat: old questions, new insights. Endocrine 23:183–188CrossRefGoogle Scholar
  34. 34.
    Kim BJ, Ahn SH, Bae SJ, Kim EH, Kim TH, Lee SH, Kim HK, Choe JW, Kim SY, Koh JM, Kim GS (2013) Association between metabolic syndrome and bone loss at various skeletal sites in postmenopausal women: a 3-year retrospective longitudinal study. Osteoporos Int 24:2243–2252CrossRefGoogle Scholar
  35. 35.
    Grobbee DE, Hackeng WH, Birkenhäger JC, Hofman A (1988) Raised plasma intact parathyroid hormone concentrations in young people with mildly raised blood pressure. Br Med J (Clin Res Ed) 296:814–816CrossRefGoogle Scholar
  36. 36.
    Hughes GS Jr, Oexmann MJ, Margolius HS, Epstein S, Bell NH (1988) Normal vitamin D and mineral metabolism in essential hypertension. Am J Med Sci 296:252–259CrossRefGoogle Scholar
  37. 37.
    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, Canadian Multicentre Osteoporosis Study Research Group (2003) Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: crosssectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res 18:784–790CrossRefGoogle Scholar
  38. 38.
    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 16:395–399CrossRefGoogle Scholar
  39. 39.
    Yang S, Nguyen ND, Center JR, Eisman JA (2014) Association between hypertension and fragility fracture: a longitudinal study. Osteoporosis Int 25:97–103CrossRefGoogle Scholar
  40. 40.
    Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, Chihara K (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217CrossRefGoogle Scholar
  41. 41.
    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 74:136–142CrossRefGoogle Scholar
  42. 42.
    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 18:1337–1344CrossRefGoogle Scholar
  43. 43.
    Dennison EM, Syddall HE, Aihie Sayer A, Martin HJ, Cooper C (2007) Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort Study. QJM 100:297–303CrossRefGoogle Scholar
  44. 44.
    Ishii S, Miyao M, Mizuno Y, Tanaka-Ishikawa M, Akishita M, Ouchi Y (2014) Association between serum uric acid and lumbar spine bone mineral density in peri- and postmenopausal Japanese women. Osteoporosis Int l25:1099–1105CrossRefGoogle Scholar
  45. 45.
    Makovey J, Macara M, Chen JS, Hayward CS, March L, Seibel MJ, Sambrook PN (2013) Serum uric acid plays a protective role for bone loss in peri- and postmenopausal women: a longitudinal study. Bone 52:400–406CrossRefGoogle Scholar
  46. 46.
    Shin JH, Kim SH, Yu SH (2014) Metabolic syndrome and chronic kidney disease as risk factors of osteoporosis. Clin Nephrol 81:1–8CrossRefGoogle Scholar
  47. 47.
    Kong X, Tang L, Ma X, Liu W, Wang Z, Cui M, Xu D (2015) Relationship between mild-to-moderate chronic kidney disease and decreased bone mineraldensity in Chinese adult population. Int Urol Nephro 47:1547–1553CrossRefGoogle Scholar

Copyright information

© The Japanese Society for Bone and Mineral Research and Springer Japan 2017

Authors and Affiliations

  1. 1.Department of Family Medicine, Kaohsiung Chang Gung Memorial HospitalChang Gung University College of MedicineKaohsiungTaiwan
  2. 2.Department of Biological SciencesNational Sun Yat-sen UniversityKaohsiungTaiwan
  3. 3.Department of Occupation MedicineKeelung Chang-Gung Memorial HospitalKeelungTaiwan

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