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Factors that characterize bone health with aging in healthy postmenopausal women

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Abstract

The exponential increase in the incidence of fragility fractures in older people is attributed to attenuation of both bone strength and neuromuscular function. Decrease in bone mineral density (BMD) does not entirely explain this increase. The objective of this study is to investigate the effect of age on various parameters related to bone health with aging, and to identify combinations of factors that collectively express the bone metabolic state in healthy postmenopausal women. Height, weight, and grip strength were measured in 135 healthy postmenopausal volunteer women. Hip BMD, biomechanical indices derived from quantitative computed tomography (QCT), cross-sectional areas of muscle and fat of the proximal thigh, and various biochemical markers of bone metabolism were measured. A smaller group of factors explanatory for bone health was identified using factor analysis and each was newly named. As a result, the factors bone mass, bone turnover, bone structure, and muscle strength had the greatest explanatory power for assessing the bone health of healthy postmenopausal women. Whereas dual X-ray absorptiometry parameters only loaded on the factor bone mass, QCT parameters loaded on both the factors bone mass and bone structure. Most bone turnover markers loaded on the factor bone turnover, but deoxypyridinoline loaded on both bone turnover and muscle strength. Age was negatively correlated with bone mass (r = −0.49, p < 0.001) and muscle strength (r = −0.67, p < 0.001). We conclude that aging is associated as much with muscle weakening as with low BMD. More attention should be paid to the effects of muscle weakening during aging in assessments of bone health.

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References

  1. Adams JE (2013) Advances in bone imaging for osteoporosis. Nat Rev Endocrinol 9:28–42

    Article  CAS  PubMed  Google Scholar 

  2. Blake GM, Fogelman I (2009) The clinical role of dual energy X-ray absorptiometry. Eur J Radiol 71:406–414

    Article  PubMed  Google Scholar 

  3. Borggrefe J, Graeff C, Nickelsen TN, Marin F, Gluer CC (2010) Quantitative computed tomographic assessment of the effects of 24 months of teriparatide treatment on 3D femoral neck bone distribution, geometry, and bone strength: results from the EUROFORS study. J Bone Miner Res 25:472–481

    Article  CAS  PubMed  Google Scholar 

  4. Cranney A, Horsley T, O’Donnell S, Weiler H, Puil L, Ooi D, Atkinson S, Ward L, Moher D, Hanley D, Fang M, Yazdi F, Garritty C, Sampson M, Barrowman N, Tsertsvadze A, Mamaladze V (2007) Effectiveness and safety of vitamin D in relation to bone health. Evid Rep Technol Assess (Full Rep) 158:1–235

    Google Scholar 

  5. Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214

    Article  CAS  PubMed  Google Scholar 

  6. Shiraki M, Kuroda T, Tanaka S, Saito M, Fukunaga M, Nakamura T (2008) Nonenzymatic collagen cross-links induced by glycoxidation (pentosidine) predicts vertebral fractures. J Bone Miner Metab 26:93–100

    Article  CAS  PubMed  Google Scholar 

  7. Salamone LM, Fuerst T, Visser M, Kern M, Lang T, Dockrell M, Cauley JA, Nevitt M, Tylavsky F, Lohman TG (2000) Measurement of fat mass using DEXA: a validation study in elderly adults. J Appl Physiol 89:345–352

    CAS  PubMed  Google Scholar 

  8. Ward SR, Lieber RL (2005) Density and hydration of fresh and fixed human skeletal muscle. J Biomech 38:2317–2320

    Article  PubMed  Google Scholar 

  9. Chen LK, Liu LK, Woo J, Assantachai P, Auyeung TW et al. (2014) Sarcopenia in Asia: consensus report of the Asian working group for sarcopenia. J Am Med Dir Assoc 15:95–101

    Article  PubMed  Google Scholar 

  10. DiGirolamo DJ, Kiel DP, Esser KA (2013) Bone and skeletal muscle: neighbors with close ties. J Bone Miner Res 28:1509–1518

    Article  PubMed  Google Scholar 

  11. Narici MV, Maganaris C, Reeves N (2005) Myotendinous alterations and effects of resistive loading in old age. Scand J Med Sci Sports 15:392–401

    Article  CAS  PubMed  Google Scholar 

  12. Wolfson L, Judge J, Whipple R, King M (1995) Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 50 Spec No: 64–67

  13. Sirola J, Tuppurainen M, Honkanen R, Jurvelin JS, Kröger H (2005) Associations between grip strength change and axial postmenopausal bone loss–a 10-year population-based follow-up study. Osteoporos Int 16:1841–1848

    Article  PubMed  Google Scholar 

  14. Horstman AM, Dillon EL, Urban RJ, Sheffield-Moore M (2012) The role of androgens and estrogens on healthy aging and longevity. J Gerontol A Biol Sci Med Sci 67:1140–1152

    Article  PubMed Central  PubMed  Google Scholar 

  15. Lofthus CM, Osnes EK, Falch JA, Kaastad TS, Kristiansen IS, Nordsletten L, Stensvold I, Meyer HE (2001) Epidemiology of hip fractures in Oslo, Norway. Bone 29:413–418

    Article  CAS  PubMed  Google Scholar 

  16. Melton LJ 3rd (1996) Epidemiology of hip fractures: implications of the exponential increase with age. Bone 18:121S–125S

    Article  PubMed  Google Scholar 

  17. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, Martin FC, Michel JP, Rolland Y, Schneider SM, Topinková E, Vandewoude M, Zamboni M, European Working Group on Sarcopenia in Older People (2010) Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people. Age Ageing 39:412–423

    Article  PubMed Central  PubMed  Google Scholar 

  18. Tanimoto Y, Watanabe M, Sun W, Sugiura Y, Tsuda Y, Kimura M, Hayashida I, Kusabiraki T, Kono K (2012) Association between sarcopenia and higher-level functional capacity in daily living in community-dwelling elderly subjects in Japan. Arch Gerontol Geriatr 55:e9–e13

    Article  PubMed  Google Scholar 

  19. Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, Berger ML (2004) Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med 164:1108–1112

    Article  PubMed  Google Scholar 

  20. Robbins JA, Schott AM, Garnero P, Delmas PD, Hans D, Meunier PJ (2005) Risk factors for hip fracture in women with high BMD: EPIDOS study. Osteoporos Int 16:149–154

    Article  CAS  PubMed  Google Scholar 

  21. Ringe JD (2012) The effect of vitamin D on falls and fractures. Scand J Clin Lab Investig Suppl 243:73–78

    Google Scholar 

  22. Ceglia L (2009) Vitamin D and its role in skeletal muscle. Curr Opin Clin Nutr Metab Care 12:628–633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Ikegami S, Kamimura M, Uchiyama S, Kato H (2011) Women with insufficient 25-hydroxyvitamin D without secondary hyperparathyroidism have altered bone turnover and greater incidence of vertebral fractures. J Orthop Sci 16:573–580

    Article  CAS  PubMed  Google Scholar 

  24. Oyen J, Apalset EM, Gjesdal CG, Brudvik C, Lie SA, Hove LM (2008) Vitamin D inadequacy is associated with low-energy distal radius fractures: a case–control study. Ann Intern Med 149:242–250

    Article  Google Scholar 

  25. Matheï C, Van Pottelbergh G, Vaes B, Adriaensen W, Gruson D, Degryse JM (2013) No relation between vitamin D status and physical performance in the oldest old: results from the Belfrail study. Age Ageing 42:186–190

    Article  PubMed  Google Scholar 

  26. Verzijl N, DeGroot J, Thorpe SR, Bank RA, Shaw JN, Lyons TJ, Bijlsma JW, Lafeber FP, Baynes JW, TeKoppele JM (2000) Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem 275:39027–39031

    Article  CAS  PubMed  Google Scholar 

  27. Haus JM, Carrithers JA, Trappe SW, Trappe TA (2007) Collagen, cross-linking, and advanced glycation end products in aging human skeletal muscle. J Appl Physiol 103:2068–2076

    Article  CAS  PubMed  Google Scholar 

  28. Vos PA, Mastbergen SC, Huisman AM, de Boer TN, DeGroot J, Polak AA, Lafeber FP (2012) In end stage osteoarthritis, cartilage tissue pentosidine levels are inversely related to parameters of cartilage damage. Osteoarthr Cartil 20:233–240

    Article  CAS  PubMed  Google Scholar 

  29. Shiraki M, Kuroda T, Shiraki Y, Tanaka S, Higuchi T, Saito M (2011) Urinary pentosidine and plasma homocysteine levels at baseline predict future fractures in osteoporosis patients under bisphosphonate treatment. J Bone Miner Metab 29:62–70

    Article  CAS  PubMed  Google Scholar 

  30. Dominguez LJ, Galioto A, Pineo A, Ferlisi A, Ciaccio M, Putignano E, Belvedere M, Costanza G, Barbagallo M (2010) Age, homocysteine, and oxidative stress: relation to hypertension and type 2 diabetes mellitus. J Am Coll Nutr 29:1–6

    Article  CAS  PubMed  Google Scholar 

  31. Yang J, Hu X, Zhang Q, Cao H, Wang J, Liu B (2012) Homocysteine level and risk of fracture: a meta-analysis and systematic review. Bone 51:376–382

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Mr. S. Sasaki from the Radiology Division, Mr. M. Sugano from Laboratory Medicine and Y. Ido, OT, and A. Takada, OT, from the Department of Rehabilitation Medicine, all at Shinshu University School of Medicine, for collecting data.

Conflict of interest

This work was supported by grants received from the following sources: the Japan Orthopaedics and Traumatology Foundation, Inc. (No. 257); the Chiyoda Health Development Agency (medical research grant); the Preventive Medical Center of Shinshu University Hospital; the Project to Promote Education, Research and Medical Care at Shinshu University Hospital; and research funding from the Josho District.

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Correspondence to Shota Ikegami.

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Ikegami, S., Uchiyama, S., Nakamura, Y. et al. Factors that characterize bone health with aging in healthy postmenopausal women. J Bone Miner Metab 33, 440–447 (2015). https://doi.org/10.1007/s00774-014-0608-4

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  • DOI: https://doi.org/10.1007/s00774-014-0608-4

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