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The association between metabolic syndrome and bone mineral density: a meta-analysis

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Abstract

Previous researches demonstrate uncertainty about the effect of metabolic syndrome (MS) on bone. We performed a meta-analysis to investigate the association of MS with bone mineral density (BMD) of spine and femoral neck (FN). In this meta-analysis, searches of Medline, Embase, Cochrane Library, Chinese biological medical database and China national knowledge infrastructure were undertaken to identify studies in humans of the association between MS and BMD. Random effects model was used for this meta-analysis. The results of our research were reported using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. A total of 11 studies (including an outlier study) with 13,122 subjects were included in our research. We detected a significant overall association of MS with increased BMD of spine (weighted mean difference, WMD = 0.027, 95 % confidence interval, CI [0.011, 0.042]) and no significant overall association of MS with BMD of FN (WMD = 0.008, CI [−0.011, 0.026]). Subgroup analyses indicated significant association between MS and increased BMD of spine in subjects whose BMD was measured by dual-energy X-ray absorptiometry (DXA) scanner manufactured by Hologic Inc., subjects diagnosed by International Diabetes Federation criteria and subjects diagnosed by National Cholesterol Education Program’s Adult Treatment Panel III (NCEP-ATP III) criteria. And significant association between MS and increased BMD of FN in Caucasian subjects, subjects whose BMD was measured by DXA scanner manufactured by Hologic Inc. and subjects diagnosed by NCEP-ATP III criteria was also found. Our meta-analysis suggests that MS has no clear influence on BMD, or its influence maybe beneficial.

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References

  1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy, Osteoporosis prevention, diagnosis, and therapy. JAMA 285(6), 785–795 (2001)

    Google Scholar 

  2. Writing Group for the ISCD Position Development Conference, Diagnosis of osteoporosis in men, premenopausal women, and children. J. Clin. Densitom. 7(1), 17–26 (2004)

    Google Scholar 

  3. J.Y. Reginster, P. Gillet, W. Ben Sedrine, G. Brands, O. Ethgen, C. de Froidmont, C. Gosset, Direct costs of hip fractures in patients over 60 years of age in Belgium. Pharmacoeconomics 15(5), 507–514 (1999)

    Article  PubMed  CAS  Google Scholar 

  4. C. Gazzaruso, An increased risk for fractures: another cause of frailty in HIV-infected subjects. Endocrine (2012). doi:10.1007/s12020-012-9640-0

    Google Scholar 

  5. M.A. Cornier, D. Dabelea, T.L. Hernandez, R.C. Lindstrom, A.J. Steig, N.R. Stob, R.E. Van Pelt, H. Wang, R.H. Eckel, The metabolic syndrome. Endocr. Rev. 29(7), 777–822 (2008). doi:10.1210/er.2008-0024

    Article  PubMed  CAS  Google Scholar 

  6. A.S. Gami, B.J. Witt, D.E. Howard, P.J. Erwin, L.A. Gami, V.K. Somers, V.M. Montori, Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J. Am. Coll. Cardiol. 49(4), 403–414 (2007). doi:10.1016/j.jacc.2006.09.032

    Article  PubMed  CAS  Google Scholar 

  7. E.S. Ford, C. Li, N. Sattar, Metabolic syndrome and incident diabetes: current state of the evidence. Diabetes Care 31(9), 1898–1904 (2008). doi:10.2337/dc08-0423

    Article  PubMed  Google Scholar 

  8. L.R. Nelson, S.E. Bulun, Estrogen production and action. J. Am. Acad. Dermatol. 45(3 Suppl), S116–S124 (2001)

    Article  PubMed  CAS  Google Scholar 

  9. H. Ohta, T. Ikeda, T. Masuzawa, K. Makita, Y. Suda, S. Nozawa, 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(2), 111–116 (1993)

    Article  PubMed  CAS  Google Scholar 

  10. L.C. Hofbauer, M. Schoppet, Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA 292(4), 490–495 (2004). doi:10.1001/jama.292.4.490

    Article  PubMed  CAS  Google Scholar 

  11. B.J. Smith, M.R. Lerner, S.Y. Bu, E.A. Lucas, J.S. Hanas, S.A. Lightfoot, R.G. Postier, M.S. Bronze, D.J. Brackett, Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone 38(3), 378–386 (2006). doi:10.1016/j.bone.2005.09.008

    Article  PubMed  CAS  Google Scholar 

  12. R.M. Campos, A. de Piano, P.L. da Silva, J. Carnier, P.L. Sanches, F.C. Corgosinho, D.C. Masquio, M. Lazaretti-Castro, L.M. Oyama, C.M. Nascimento, L. Tock, M.T. de Mello, S. Tufik, A.R. Damaso, The role of pro/anti-inflammatory adipokines on bone metabolism in NAFLD obese adolescents: effects of long-term interdisciplinary therapy. Endocrine (2012). doi:10.1007/s12020-012-9613-3

    PubMed  Google Scholar 

  13. S. Cvijetic, M. Pavlovic, D. Pasalic, S. Dodig, Ultrasound bone measurement in an older population with metabolic syndrome. Aging Clin Exp Res 23(1), 29–34 (2011)

    PubMed  CAS  Google Scholar 

  14. D.N. Binici, N. Gunes, Risk factors leading to reduced bone mineral density in hemodialysis patients with metabolic syndrome. Ren. Fail. 32(4), 469–474 (2010). doi:10.3109/08860221003675260

    Article  PubMed  CAS  Google Scholar 

  15. M. Kinjo, S. Setoguchi, D.H. Solomon, 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 (2007). doi:10.1210/jc.2007-0757

    Article  PubMed  CAS  Google Scholar 

  16. Y.H. Tseng, K.C. Huang, M.L. Liu, W.T. Shu, W.H. Sheu, Association between metabolic syndrome (MS) and bone mineral loss: a cross-sectional study in Puli Township in Taiwan. Arch. Gerontol. Geriatr. 49(Suppl 2), S37–S40 (2009). doi:10.1016/S0167-4943(09)70011-1

    Article  PubMed  Google Scholar 

  17. T. Yamaguchi, I. Kanazawa, M. Yamamoto, S. Kurioka, M. Yamauchi, S. Yano, T. Sugimoto, Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone 45(2), 174–179 (2009). doi:10.1016/j.bone.2009.05.003

    Article  PubMed  CAS  Google Scholar 

  18. L.A. Ahmed, H. Schirmer, G.K. Berntsen, V. Fonnebo, R.M. Joakimsen, Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromso study. Osteoporos. Int. 17(3), 426–432 (2006). doi:10.1007/s00198-005-0003-z

    Article  PubMed  CAS  Google Scholar 

  19. G. Iacobellis, M. Iorio, N. Napoli, D. Cotesta, L. Zinnamosca, C. Marinelli, L. Petramala, S. Minisola, E. D’Erasmo, C. Letizia, Relation of adiponectin, visfatin and bone mineral density in patients with metabolic syndrome. J. Endocrinol. Investig. 34(1), e12–e15 (2011). doi:10.3275/7170

    CAS  Google Scholar 

  20. H.T. Lee, J. Shin, Y.H. Lim, B.K. Kim, Y.T. Kim, J.U. Lee, S. Hong, S.Y. Song, S.H. Cho, The relationship between coronary artery calcification and bone mineral density in patients according to their metabolic syndrome status. Korean Circ. J. 41(2), 76–82 (2011). doi:10.4070/kcj.2011.41.2.76

    Article  PubMed  Google Scholar 

  21. L.J. Lu, F. Nayeem, K.E. Anderson, J.J. Grady, M. Nagamani, Lean body mass, not estrogen or progesterone, predicts peak bone mineral density in premenopausal women. J. Nutr. 139(2), 250–256 (2009). doi:10.3945/jn.108.098954

    PubMed  CAS  Google Scholar 

  22. J. Lidfeldt, L. Holmdahl, G. Samsioe, C. Nerbrand, P. Nyberg, B. Schersten, C.D. Agardh, The influence of hormonal status and features of the metabolic syndrome on bone density: a population-based study of Swedish women aged 50 to 59 years. The women’s health in the Lund area study. Metabolism 51(2), 267–270 (2002)

    Article  PubMed  CAS  Google Scholar 

  23. Y.K. Jeon, J.G. Lee, S.S. Kim, B.H. Kim, S.J. Kim, Y.K. Kim, I.J. Kim, Association between bone mineral density and metabolic syndrome in pre- and postmenopausal women. Endocr. J. 58(2), 87–93 (2011)

    Article  PubMed  Google Scholar 

  24. P. Szulc, A. Varennes, P.D. Delmas, J. Goudable, R. Chapurlat, Men with metabolic syndrome have lower bone mineral density but lower fracture risk—the MINOS study. J. Bone Miner. Res. 25(6), 1446–1454 (2010). doi:10.1002/jbmr.13

    Article  PubMed  Google Scholar 

  25. K.K. Park, S.J. Kim, E.S. Moon, Association between bone mineral density and metabolic syndrome in postmenopausal Korean women. Gynecol. Obstet. Investig. 69(3), 145–152 (2010). doi:10.1159/000264665

    Article  Google Scholar 

  26. D. von Muhlen, S. Safii, S.K. Jassal, J. Svartberg, E. Barrett-Connor, Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo study. Osteoporos. Int. 18(10), 1337–1344 (2007). doi:10.1007/s00198-007-0385-1

    Article  Google Scholar 

  27. D.K. Hwang, H.J. Choi, The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos. Int. 21(3), 425–431 (2010). doi:10.1007/s00198-009-0990-2

    Article  PubMed  Google Scholar 

  28. M. Boyanov, D. Bakalov, Z. Boneva, Bone mineral density in men with and without the metabolic syndrome. Aging Male 12(2–3), 62–65 (2009). doi:10.1080/13685530903150812

    Article  PubMed  CAS  Google Scholar 

  29. J.L. Hernandez, J.M. Olmos, E. Pariente, J. Martinez, C. Valero, P. Garcia-Velasco, D. Nan, J. Llorca, J. Gonzalez-Macias, Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17(5), 955–961 (2010). doi:10.1097/gme.0b013e3181e39a15

    Article  PubMed  Google Scholar 

  30. S. Yaturu, S. Humphrey, C. Landry, S.K. Jain, Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med. Sci. Monit. 15(1), CR5–CR9 (2009)

    PubMed  Google Scholar 

  31. H.Y. Kim, J.W. Choe, H.K. Kim, S.J. Bae, B.J. Kim, S.H. Lee, J.M. Koh, K.O. Han, H.M. Park, G.S. Kim, Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif. Tissue Int. 86(5), 350–358 (2010). doi:10.1007/s00223-010-9347-2

    Article  PubMed  CAS  Google Scholar 

  32. Y.-J. Zhang, W. Zhao, H. Zhang, X.-M. Wu, L.-J. Jiang, X.-C. Song, M. Li, Effect of metabolic syndrome on bone mineral density of male patients with type 2 diabetes. TianJin Med. J. 38(3), 230–232 (2010)

    Google Scholar 

  33. Y.-J. Zhang, W. Zhao, H. Zhang, J. Liu, X.-Q. Chen, S.-S. Cui, L. Zhang, Analysis of the related factors of bone mineral density in female patients with type 2 diabetes complicated metabolic syndrome. Chin. J. Prev. Control Chronic Dis. 18(05), 481–482 (2010)

    CAS  Google Scholar 

  34. D.T. Felson, Y. Zhang, M.T. Hannan, J.J. Anderson, Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J. Bone Miner. Res. 8(5), 567–573 (1993). doi:10.1002/jbmr.5650080507

    Article  PubMed  CAS  Google Scholar 

  35. R. Marcus, G. Greendale, B.A. Blunt, T.L. Bush, S. Sherman, R. Sherwin, H. Wahner, B. Wells, Correlates of bone mineral density in the postmenopausal estrogen/progestin interventions trial. J. Bone Miner. Res. 9(9), 1467–1476 (1994). doi:10.1002/jbmr.5650090920

    Article  PubMed  CAS  Google Scholar 

  36. C. De Laet, J.A. Kanis, A. Oden, H. Johanson, O. Johnell, P. Delmas, J.A. Eisman, H. Kroger, S. Fujiwara, P. Garnero, E.V. McCloskey, D. Mellstrom, L.J. Melton III, P.J. Meunier, H.A. Pols, J. Reeve, A. Silman, A. Tenenhouse, Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos. Int. 16(11), 1330–1338 (2005). doi:10.1007/s00198-005-1863-y

    Article  PubMed  Google Scholar 

  37. J.M. Gimble, M.E. Nuttall, Bone and fat: old questions, new insights. Endocrine 23(2–3), 183–188 (2004). doi:10.1385/ENDO:23:2-3:183

    Article  PubMed  CAS  Google Scholar 

  38. S.L. Edelstein, E. Barrett-Connor, Relation between body size and bone mineral density in elderly men and women. Am. J. Epidemiol. 138(3), 160–169 (1993)

    PubMed  CAS  Google Scholar 

  39. E.A. Jankowska, E. Rogucka, M. Medras, 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 (2001)

    Article  PubMed  CAS  Google Scholar 

  40. R. Blaauw, E.C. Albertse, S. Hough, Body fat distribution as a risk factor for osteoporosis. S. Afr. Med. J. 86(9), 1081–1084 (1996)

    PubMed  CAS  Google Scholar 

  41. C. Torti, G. Mazziotti, P.A. Soldini, E. Foca, R. Maroldi, D. Gotti, G. Carosi, A. Giustina, High prevalence of radiological vertebral fractures in HIV-infected males. Endocrine (2011). doi:10.1007/s12020-011-9586-7

    PubMed  Google Scholar 

  42. S.S. Moon, Y.S. Lee, S.W. Kim, Association of nonalcoholic fatty liver disease with low bone mass in postmenopausal women. Endocrine (2012). doi:10.1007/s12020-012-9639-6

    PubMed  Google Scholar 

  43. A.H. Holmberg, P.M. Nilsson, J.A. Nilsson, K. Akesson, The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women. J. Clin. Endocrinol. Metab. 93(3), 815–822 (2008). doi:10.1210/jc.2007-0843

    Article  PubMed  CAS  Google Scholar 

  44. I. Kanazawa, T. Yamaguchi, M. Yamamoto, M. Yamauchi, S. Yano, T. Sugimoto, Combination of obesity with hyperglycemia is a risk factor for the presence of vertebral fractures in type 2 diabetic men. Calcif. Tissue Int. 83(5), 324–331 (2008). doi:10.1007/s00223-008-9178-6

    Article  PubMed  CAS  Google Scholar 

  45. K. Agbaht, A. Gurlek, J. Karakaya, M. Bayraktar, Circulating adiponectin represents a biomarker of the association between adiposity and bone mineral density. Endocrine 35(3), 371–379 (2009). doi:10.1007/s12020-009-9158-2

    Article  PubMed  CAS  Google Scholar 

  46. G. Mazziotti, M. Gola, A. Bianchi, T. Porcelli, A. Giampietro, V. Cimino, M. Doga, C. Gazzaruso, L. De Marinis, A. Giustina, Influence of diabetes mellitus on vertebral fractures in men with acromegaly. Endocrine 40(1), 102–108 (2011). doi:10.1007/s12020-011-9486-x

    Article  PubMed  CAS  Google Scholar 

  47. D.E. Grobbee, W.H. Hackeng, J.C. Birkenhager, A. Hofman, Raised plasma intact parathyroid hormone concentrations in young people with mildly raised blood pressure. Br. Med. J. (Clin. Res. Ed.) 296(6625), 814–816 (1988)

    Article  CAS  Google Scholar 

  48. G.S. Hughes Jr, M.J. Oexmann, H.S. Margolius, S. Epstein, N.H. Bell, Normal vitamin D and mineral metabolism in essential hypertension. Am. J. Med. Sci. 296(4), 252–259 (1988)

    PubMed  Google Scholar 

  49. D.A. Hanley, J.P. Brown, A. Tenenhouse, W.P. Olszynski, G. Ioannidis, C. Berger, J.C. Prior, L. Pickard, T.M. Murray, T. Anastassiades, S. Kirkland, C. Joyce, L. Joseph, A. Papaioannou, S.A. Jackson, S. Poliquin, J.D. Adachi, 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(4), 784–790 (2003). doi:10.1359/jbmr.2003.18.4.784

    Article  PubMed  CAS  Google Scholar 

  50. M.E. Mussolino, R.F. Gillum, 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 (2006). doi:10.1016/j.annepidem.2005.06.051

    Article  PubMed  Google Scholar 

  51. S. Xu, J.J. Yu, Beneath the minerals, a layer of round lipid particles was identified to mediate collagen calcification in compact bone formation. Biophys. J. 91(11), 4221–4229 (2006). doi:10.1529/biophysj.105.075804

    Article  PubMed  CAS  Google Scholar 

  52. S. Adami, V. Braga, M. Zamboni, D. Gatti, M. Rossini, J. Bakri, E. Battaglia, Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif. Tissue Int. 74(2), 136–142 (2004). doi:10.1007/s00223-003-0050-4

    Article  PubMed  CAS  Google Scholar 

  53. T. Yamaguchi, T. Sugimoto, S. Yano, M. Yamauchi, H. Sowa, Q. Chen, K. Chihara, Plasma lipids and osteoporosis in postmenopausal women. Endocr. J. 49(2), 211–217 (2002)

    Article  PubMed  CAS  Google Scholar 

  54. E.M. Dennison, H.E. Syddall, A. Aihie Sayer, H.J. Martin, C. Cooper, Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort study. QJM 100(5), 297–303 (2007). doi:10.1093/qjmed/hcm023

    Article  PubMed  CAS  Google Scholar 

  55. W.Y. Fujimoto, Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet. Med. 13(9 Suppl 6), S7–S10 (1996)

    PubMed  CAS  Google Scholar 

  56. N. Abate, M. Chandalia, The impact of ethnicity on type 2 diabetes. J. Diabetes Complicat. 17(1), 39–58 (2003)

    Article  PubMed  Google Scholar 

  57. N.A. Pocock, K.A. Noakes, M. Griffiths, N. Bhalerao, P.N. Sambrook, J.A. Eisman, J. Freund, A comparison of longitudinal measurements in the spine and proximal femur using lunar and hologic instruments. J. Bone Miner. Res. 12(12), 2113–2118 (1997). doi:10.1359/jbmr.1997.12.12.2113

    Article  PubMed  CAS  Google Scholar 

  58. J. Makovey, V. Naganathan, P. Sambrook, Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos. Int. 16(12), 1495–1505 (2005). doi:10.1007/s00198-005-1841-4

    Article  PubMed  Google Scholar 

  59. G. Mazziotti, J. Bilezikian, E. Canalis, D. Cocchi, A. Giustina, New understanding and treatments for osteoporosis. Endocrine 41(1), 58–69 (2012). doi:10.1007/s12020-011-9570-2

    Article  PubMed  CAS  Google Scholar 

  60. Y. Hamada, S. Kitazawa, R. Kitazawa, K. Kono, S. Goto, H. Komaba, H. Fujii, Y. Yamamoto, H. Yamamoto, M. Usami, M. Fukagawa, The effects of the receptor for advanced glycation end products (RAGE) on bone metabolism under physiological and diabetic conditions. Endocrine 38(3), 369–376 (2010). doi:10.1007/s12020-010-9390-9

    Article  PubMed  CAS  Google Scholar 

  61. J.A. Pasco, M.J. Henry, S. Korn, G.C. Nicholson, M.A. Kotowicz, The metabolic syndrome and bone mineral density in a random sample of Australian men. JMHG. 4(3), 298–299 (2007)

    Google Scholar 

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Acknowledgments

This work was supported by National Natural Science foundation of Hebei Province, China (no: C2009001179).

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  1. Department of Endocrinology, The Third Hospital of Hebei Medical University, 139 Ziqiang Road, Shijiazhuang, 050000, Hebei Province, China

    Peng Xue & Yukun Li

  2. Department of Social Medicine, School of Public Health, Hebei Medical University, 361 East Zhongshan Road, Shijiazhuang, 050000, Hebei Province, China

    Ping Gao

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Xue, P., Gao, P. & Li, Y. The association between metabolic syndrome and bone mineral density: a meta-analysis. Endocrine 42, 546–554 (2012). https://doi.org/10.1007/s12020-012-9684-1

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