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Bone quantitative ultrasound measurements in relation to the metabolic syndrome and type 2 diabetes mellitus in a cohort of elderly subjects at high risk of cardiovascular disease from the predimed study

  • JNHA: Geriatric Science
  • Published:
The journal of nutrition, health & aging

Abstract

Objective

The aim of this study is to determine whether metabolic syndrome, its individual components, or the presence of type 2 diabetes mellitus are associated with a better bone status estimated by quantitative ultrasound at the calcaneus.

Design

Cross-sectional study.

Setting

Outpatient clinics.

Participants

251 elderly subjects at high cardiovascular risk from the PREDIMED study were included.

Measurements

MetS was defined according to the ATPIII diagnosis criteria. Calcaneus quantitative ultrasound (QUS) assessment was performed using the Sahara system.

Results

Subjects with MetS showed significantly lower 24-hour urinary deoxypyridinoline/creatinine (u-DPD/creatinine) levels and higher broadband ultrasound attenuation, and a tendency to higher bone mineral density (BMD) and quantitative ultrasound index (QUI) than their counterparts. Individuals with type 2 diabetes mellitus (T2DM) showed a significantly higher bone broadband ultrasound attenuation (BUA) and QUI than their non-diabetic counterparts, despite they shown a higher prevalence of osteoporotic fractures. Multiple linear regression analyses showed that quantitative ultrasound parameters were positively associated with the metabolic syndrome and T2DM. Of the bone biochemical markers, only u-DPD/creatinine was related to MetS, abdominal obesity, hypertriglyceridemia component of the MetS, and the number of features that define the MetS.

Conclusion

This is the first study showing a positive association between MetS or T2DM with better bone status and lower bone resorption markers measured by quantitative ultrasound. Our results suggest that metabolic abnormalities have a positive effect on healthy bone in elderly subjects at high risk of cardiovascular disease.

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References

  1. McFarlane SI, Muniyappa R, Shin JJ, Bahtiyar G, Sowers JR (2004) Osteoporosis and cardiovascular disease: brittle bones and boned arteries, is there a link? Endocrine 23:1–10.

    Article  PubMed  CAS  Google Scholar 

  2. Frye MA, Melton LJ, Bryant SC, Fitzpatrick LA, Wahner HW, Schwartz RS, et al (1992) Osteoporosis and calcification of the aorta. Bone Miner 19:185–194.

    Article  PubMed  CAS  Google Scholar 

  3. Ahmed LA, Schirmer H, Berntsen GK, Fonnebo V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int 17:426–432.

    Article  PubMed  CAS  Google Scholar 

  4. 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 92:4161–4164.

    Article  PubMed  CAS  Google Scholar 

  5. Boyanov M, Bakalov D, Boneva Z (2009) Bone mineral density in men with and without the metabolic syndrome. Aging Male 12:62–65.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  7. 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 18:1337–1344.

    Article  Google Scholar 

  8. Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431.

    Article  PubMed  Google Scholar 

  9. Yaturu S, Humphrey S, Landry C, Jain SK (2009) Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit 15:CR5–9.

    PubMed  Google Scholar 

  10. Kim HY, Choe JW, Kim HK, Bae SJ, Kim BJ, Lee SH, et al (2010) Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif Tissue Int 86:350–358.

    Article  PubMed  CAS  Google Scholar 

  11. Tseng YH, Huang KC, Liu ML, Shu WT, Sheu WH (2009) Association between metabolic syndrome (MS) and bone mineral loss: a cross-sectional study in Puli Township in Taiwan. Arch Gerontol Geriatr 49Suppl 2:S37–S40.

    Article  PubMed  Google Scholar 

  12. Siris ES, Miller PD, Barrett-Connor E, Faulkner KG, Wehren LE, Abbott TA, et al (2001) Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the National Osteoporosis Risk Assessment. JAMA 286:2815–2822.

    Article  PubMed  CAS  Google Scholar 

  13. 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 33:384–389.

    Article  PubMed  CAS  Google Scholar 

  14. Barrett-Connor E, Holbrook TL (1992) Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337.

    Article  PubMed  CAS  Google Scholar 

  15. Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T (1993) Bone mineral density measured by dual energy x-ray absorptiometry in patients with noninsulin-dependent diabetes mellitus. Bone 14:29–33.

    Article  PubMed  CAS  Google Scholar 

  16. van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med 122:409–414.

    PubMed  Google Scholar 

  17. Forsen L, Meyer HE, Midthjell K, Edna TH (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42:920–925.

    Article  PubMed  CAS  Google Scholar 

  18. Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, et al (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217.

    Article  PubMed  CAS  Google Scholar 

  19. Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J, et al (2004) Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int 74:136–142.

    Article  PubMed  CAS  Google Scholar 

  20. Jones DH, Kong YY, Penninger JM (2002) Role of RANKL and RANK in bone loss and arthritis. Ann Rheum Dis 61Suppl 2:ii32–9.

    PubMed  CAS  Google Scholar 

  21. Moris M, Peretz A, Tjeka R, Negaban N, Wouters M, Bergmann P (1995) Quantitative ultrasound bone measurements: normal values and comparison with bone mineral density by dual X-ray absorptiometry. Calcif Tissue Int 57:6–10.

    Article  PubMed  CAS  Google Scholar 

  22. Marin F, Gonzalez-Macias J, Diez-Perez A, Palma S, Delgado-Rodriguez M (2006) Relationship between bone quantitative ultrasound and fractures: a meta-analysis. J Bone Miner Res 21:1126–1135.

    Article  PubMed  Google Scholar 

  23. Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvado J, Ruiz-Gutierrez V, Covas MI, et al (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11.

    PubMed  Google Scholar 

  24. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, et al (2009) 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 120:1640–1645.

    Article  PubMed  CAS  Google Scholar 

  25. Fernandez-Ballart JD, Pinol JL, Zazpe I, Corella D, Carrasco P, Toledo E, et al (2010) Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain. Br J Nutr: 1–9.

  26. Elosua R, Marrugat J, Molina L, Pons S, Pujol E (1994) Validation of the Minnesota Leisure Time Physical Activity Questionnaire in Spanish men. The MARATHOM Investigators. Am J Epidemiol 139:1197–1209.

    PubMed  CAS  Google Scholar 

  27. Elosua R, Garcia M, Aguilar A, Molina L, Covas MI, Marrugat J (2000) Validation of the Minnesota Leisure Time Physical Activity Questionnaire In Spanish Women. Investigators of the MARATDON Group. Med Sci Sports Exerc 32:1431–1437.

    Article  PubMed  CAS  Google Scholar 

  28. American Diabetes Association (2009) Diagnosis and classification of diabetes mellitus. Diabetes Care 32Suppl 1:S62–7.

    Article  Google Scholar 

  29. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502.

    PubMed  CAS  Google Scholar 

  30. Sosa M, Saavedra P, Munoz-Torres M, Alegre J, Gomez C, Gonzalez-Macias J, et al (2002) Quantitative ultrasound calcaneus measurements: normative data and precision in the spanish population. Osteoporos Int 13:487–492.

    Article  PubMed  CAS  Google Scholar 

  31. Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444.

    Article  PubMed  CAS  Google Scholar 

  32. Sosa M, Saavedra P, Jodar E, Lozano-Tonkin C, Quesada JM, Torrijos A, et al (2009) Bone mineral density and risk of fractures in aging, obese post-menopausal women with type 2 diabetes. The GIUMO Study. Aging Clin Exp Res 21:27–32.

    PubMed  Google Scholar 

  33. 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 34:399–406

    Article  PubMed  Google Scholar 

  34. Njeh CF, Fuerst T, Diessel E, Genant HK (2001) Is quantitative ultrasound dependent on bone structure? A reflection. Osteoporos Int 12:1–15.

    PubMed  CAS  Google Scholar 

  35. Krieg MA, Barkmann R, Gonnelli S, Stewart A, Bauer DC, Del Rio Barquero L, et al (2008) Quantitative ultrasound in the management of osteoporosis: the 2007 ISCD Official Positions. J Clin Densitom 11:163–187.

    Article  PubMed  Google Scholar 

  36. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, et al (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363.

    Article  PubMed  CAS  Google Scholar 

  37. Schwartz AV (2003) Diabetes Mellitus: Does it Affect Bone? Calcif Tissue Int 73:515–519.

    Article  PubMed  CAS  Google Scholar 

  38. Miyata T, Notoya K, Yoshida K, Horie K, Maeda K, Kurokawa K, et al (1997) Advanced glycation end products enhance osteoclast-induced bone resorption in cultured mouse unfractionated bone cells and in rats implanted subcutaneously with devitalized bone particles. J Am Soc Nephrol 8:260–270.

    PubMed  CAS  Google Scholar 

  39. De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P, et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338.

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  41. Janghorbani M, Van Dam RM, Willett WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Human Nutrition Unit, Facultat de Medicina i Ciències de la Salut, IISPV, Universitat Rovira i Virgili, Reus, Spain

    Mònica Bulló, M. Garcia-Aloy, J. Basora & J. Salas-Salvado

  2. CIBERobn Fisiopatología de la Obesidad y Nutrición, Instituto de Salud Carlos III, Madrid, Spain

    Mònica Bulló, M. Garcia-Aloy, J. Basora, M. I. Covas & J. Salas-Salvado

  3. Municipal Institute for Medical Research (IMIM), Barcelona, Spain

    M. I. Covas

  4. Human Nutrition Unit, Faculty of Medicine of Reus, University Rovira i Virgili, C/ Sant Llorenç 21, 43201, Reus, Spain

    Mònica Bulló

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  5. J. Salas-Salvado
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Bulló, M., Garcia-Aloy, M., Basora, J. et al. Bone quantitative ultrasound measurements in relation to the metabolic syndrome and type 2 diabetes mellitus in a cohort of elderly subjects at high risk of cardiovascular disease from the predimed study. J Nutr Health Aging 15, 939–944 (2011). https://doi.org/10.1007/s12603-011-0046-0

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  • DOI: https://doi.org/10.1007/s12603-011-0046-0

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