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Assessment of trabecular bone score (TBS) in overweight/obese men: effect of metabolic and anthropometric factors

  • Endocrine Methods and Techniques
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Abstract

The “trabecular bone score” (TBS) indirectly explores bone quality, independently of bone mineral density (BMD). We investigated the effects of anthropometric and metabolic parameters on TBS in 87 overweight/obese men. We assessed BMD and TBS by DXA, and some parameters of glucose metabolism, sex-and calciotropic hormone levels. Regression models were adjusted for either age and BMI, or age and waist circumference, or age and waist/hip ratio, also considering BMI >35 (y/n) and metabolic syndrome (MS) (y/n). Correlations between TBS and parameters studied were higher when correcting for waist circumference, although not significant in subjects with BMI >35. The analysis of covariance showed that the same model always had a higher adjusted r-square index. BMD at lumbar spine and total hip, fasting glucose, bioavailable testosterone, and sex hormone-binding globulin are the only covariates having a significant effect (p < 0.05) on the variations of TBS. The presence of MS negatively affected only the association between TBS and BMD at total hip. We did not find any significant effect of BMI >35 on TBS values or significant interaction terms between each covariate and either BMI >35 or the presence of MS. Obesity negatively affected TBS, despite unchanged BMD. Alterations of glucose homeostasis and sex hormone levels seem to influence this relationship, while calciotropic hormones have no role. The effect of waist circumference on TBS is more pronounced than that of BMI.

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References

  1. B.C. Silva, W.D. Leslie, H. Resch, O. Lamy, O. Lesnyak, N. Binkley, E.V. McCloskey, J.A. Kanis, J.P. Bilezikian, Trabecular bone score: a non-invasive analytical method based upon the DXA image. J. Bone Miner. Res. 29, 518–530 (2014)

    Article  PubMed  Google Scholar 

  2. B.C. Silva, S.B. Broy, S. Boutroy, J.T. Schousboe, J.A. Shepherd, W.D. Leslie, Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD Official Positions Part 2: trabecular bone score. J. Clin. Densitom. 18, 309–330 (2015)

    Article  PubMed  Google Scholar 

  3. V. Bousson, C. Bergot, B. Sutter, P. Levitz, B. Cortet, Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos. Int. 23, 1489–1501 (2012)

    Article  CAS  PubMed  Google Scholar 

  4. K. Briot, S. Paternotte, S. Kolta, R. Eastell, D.M. Reid, D. Felsenberg, C.C. Glüer, C. Roux, Added value of trabecular bone score to bone mineral density for prediction of osteoporotic fractures in postmenopausal women: the OPUS study. Bone 57, 232–236 (2013)

    Article  PubMed  Google Scholar 

  5. J. Touvier, R. Winzenrieth, H. Johansson, J.P. Roux, J. Chaintreuil, H. Toumi, R. Jennane, D. Hans, E. Lespessailles, Fracture discrimination by combined bone mineral density (BMD) and microarchitectural texture analysis. Calcif. Tissue Int. 96, 274–283 (2015)

    Article  CAS  PubMed  Google Scholar 

  6. N.C. Harvey, C.C. Glüer, N. Binkley, E.V. McCloskey, M.L. Brandi, C. Cooper, D. Kendler, O. Lamy, A. Laslop, B.M. Camargos, J.Y. Reginster, R. Rizzoli, J.A. Kanis, Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78, 216–224 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. E. Romagnoli, C. Cipriani, I. Nofroni, C. Castro, M. Angelozzi, A. Scarpiello, J. Pepe, D. Diacinti, S. Piemonte, V. Carnevale, S. Minisola, “Trabecular bone score” (TBS): an indirect measure of bone micro-architecture in postmenopausal patients with primary hyperparathyroidism. Bone 53, 154–159 (2013)

    Article  PubMed  Google Scholar 

  8. Zhukouskaya, V.V., Eller-Vainicher, C., Gaudio, A., Privitera, F., Cairoli, E., Ulivieri, F.M., Palmieri, S., Morelli, V., Grancini, V., Orsi, E., Masserini, B., Spada, A.M., Fiore, C.E., Chiodini, I.: The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients. Osteoporos. Int. Jul 3 [Epub ahead of print] (2015)

  9. F.M. Ulivieri, B.C. Silva, F. Sardanelli, D. Hans, J.P. Bilezikian, R. Caudarella, Utility of the trabecular bone score (TBS) in secondary osteoporosis. Endocrine 47, 435–448 (2014)

    Article  CAS  PubMed  Google Scholar 

  10. C. Senn, B. Günther, A.W. Popp, R. Perrelet, D. Hans, K. Lippuner, Comparative effects of teriparatide and ibandronate on spine bone mineral density (BMD) and microarchitecture (TBS) in postmenopausal women with osteoporosis: a 2-year open-label study. Osteoporos. Int. 25, 1945–1951 (2014)

    Article  CAS  PubMed  Google Scholar 

  11. S. Di Gregorio, L. Del Rio, J. Rodriguez-Tolra, E. Bonel, M. García, R. Winzenrieth, Comparison between different bone treatments on areal bone mineral density (aBMD) and bone microarchitectural texture as assessed by the trabecular bone score (TBS). Bone 75, 138–143 (2015)

    Article  PubMed  Google Scholar 

  12. W.D. Leslie, B. Aubry-Rozier, L.M. Lix, S.N. Morin, S.R. Majumdar, D. Hans, Spine bone texture assessed by trabecular bone score (TBS) predicts osteoporotic fractures in men: the Manitoba Bone Density Program. Bone 67, 10–14 (2014)

    Article  CAS  PubMed  Google Scholar 

  13. E. Leib, R. Winzenrieth, B. Aubry-Rozier, D. Hans, Vertebral microarchitecture and fragility fracture in men: a TBS study. Bone 62, 51–55 (2014)

    Article  CAS  PubMed  Google Scholar 

  14. Schousboe, J.T., Vo, T., Taylor, B.C., Cawthon, P.M., Schwartz, A.V., Bauer, D.C., Orwoll, E.S., Lane, N.E., Barrett-Connor, E., Ensrud, K.E.; Osteoporotic Fractures in Men (MrOS) Study Research Group: Prediction of incident major osteoporotic and hip fractures by Trabecular Bone Score (TBS) and prevalent radiographic vertebral fracture in older men. J. Bone Miner. Res. Sep 17 [Epub ahead of print] (2015)

  15. K.G. Alberti, R.H. Eckel, S.M. Grundy, P.Z. Zimmet, J.I. Cleeman, K.A. Donato, J.C. Fruchart, W.P. James, C.M. Loria, S.C. Smith Jr, International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; International Association for the Study of Obesity: 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 (2009)

    Article  CAS  PubMed  Google Scholar 

  16. A. Vermeulen, L. Verdonck, J.M. Kaufman, A critical evaluation of simple methods for the estimation of free testosterone in serum. J. Clin. Endocrinol. Metab. 84, 3666–3672 (1999)

    Article  CAS  PubMed  Google Scholar 

  17. J.H. Kim, H.J. Choi, E.J. Ku, K.M. Kim, S.W. Kim, N.H. Cho, C.S. Shin, Trabecular bone score as an indicator for skeletal deterioration in diabetes. J. Clin. Endocrinol. Metab. 100, 475–482 (2015)

    Article  CAS  PubMed  Google Scholar 

  18. V. Carnevale, E. Romagnoli, L. D’Erasmo, E. D’Erasmo, Bone damage in type 2 diabetes mellitus. Nutr. Metab. Cardiovasc. Dis. 24, 1151–1157 (2014)

    Article  CAS  PubMed  Google Scholar 

  19. M.C. Zillikens, A.G. Uitterlinden, J.P. van Leeuwen, A.L. Berends, P. Henneman, K.W. van Dijk, B.A. Oostra, C.M. van Duijn, H.A. Pols, F. Rivadeneira, The role of body mass index, insulin, and adiponectin in the relation between fat distribution and bone mineral density. Calcif. Tissue Int. 86, 116–125 (2010)

    Article  CAS  PubMed  Google Scholar 

  20. Y.H. Kim, K.H. Cho, Y.S. Choi, S.M. Kim, G.E. Nam, S.H. Lee, B.J. Ko, Y.G. Park, K.D. Han, K.S. Lee, D.H. Kim, Low bone mineral density is associated with metabolic syndrome in South Korean men but not in women: the 2008–2010 Korean National Health and Nutrition Examination Survey. Arch. Osteoporos. 8, 142 (2013)

    Article  PubMed  Google Scholar 

  21. J. Zhou, Q. Zhang, X. Yuan, J. Wang, C. Li, H. Sheng, S. Qu, H. Li, Association between metabolic syndrome and osteoporosis: a meta-analysis. Bone 57, 30–35 (2013)

    Article  PubMed  Google Scholar 

  22. M.O. Premaor, J.E. Compston, F. Fina Avilés, A. Pagès-Castellà, X. Nogués, A. Díez-Pérez, D. Prieto-Alhambra, The association between fracture site and obesity in men: a population-based cohort study. J. Bone Miner. Res. 28, 1771–1777 (2013)

    Article  PubMed  Google Scholar 

  23. W.D. Leslie, M.A. Krieg, D. Hans, Manitoba Bone Density Program: clinical factors associated with trabecular bone score. J. Clin. Densitom. 16, 374–379 (2013)

    Article  PubMed  Google Scholar 

  24. W.D. Leslie, B. Aubry-Rozier, O. Lamy, D. Hans, Manitoba Bone Density Program: TBS (trabecular bone score) and diabetes-related fracture risk. J. Clin. Endocrinol. Metab. 98, 602–609 (2013)

    Article  CAS  PubMed  Google Scholar 

  25. M.A. Bredella, E. Lin, A.V. Gerweck, M.G. Landa, B.J. Thomas, M. Torriani, M.L. Bouxsein, K.K. Miller, Determinants of bone microarchitecture and mechanical properties in obese men. J. Clin. Endocrinol. Metab. 97, 4115–4122 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. S. Gonnelli, C. Caffarelli, L. Tanzilli, C. Alessi, M.D. Tomai Pitinca, S. Rossi, M.S. Campagna, R. Nuti, The associations of body composition and fat distribution with bone mineral density in elderly Italian men and women. J. Clin. Densitom. 16, 168–177 (2013)

    Article  PubMed  Google Scholar 

  27. L.H. Cui, M.H. Shin, S.S. Kweon, J.S. Choi, J.A. Rhee, Y.H. Lee, H.S. Nam, S.K. Jeong, K.S. Park, S.Y. Ryu, S.W. Choi, Sex-related differences in the association between waist circumference and bone mineral density in a Korean population. BMC Musculoskelet. Disord. 15, 326 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  28. C. Caffarelli, C. Alessi, R. Nuti, S. Gonnelli, Divergent effects of obesity on fragility fractures. Clin. Interv. Aging 9, 1629–1636 (2014)

    PubMed  PubMed Central  Google Scholar 

  29. Kim, J.H., Choi, H.J., Ku, E.J., Hong, A.R., Kim, K.M., Kim, S.W., Cho, N.H., Shin, C.S.: Regional body fat depots differently affect bone microarchitecture in postmenopausal Korean women. Osteoporos. Int. Oct 16, [Epub ahead of print] (2015)

  30. M. Bekaert, Y. Van Nieuwenhove, P. Calders, C.A. Cuvelier, A.H. Batens, J.M. Kaufman, D.M. Ouwens, J.B. Ruige, Determinants of testosterone levels in human male obesity. Endocrine 50, 202–211 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Elisabetta Romagnoli.

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Elisabetta Romagnoli, Carla Lubrano, Vincenzo Carnevale, Daniela Costantini, Luciano Nieddu, Susanna Morano, Silvia Migliaccio, Lucio Gnessi, and Andrea Lenzi declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Institutional and/or National Research Committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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E. Romagnoli and C. Lubrano have contributed equally to this work.

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Romagnoli, E., Lubrano, C., Carnevale, V. et al. Assessment of trabecular bone score (TBS) in overweight/obese men: effect of metabolic and anthropometric factors. Endocrine 54, 342–347 (2016). https://doi.org/10.1007/s12020-016-0857-1

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  • DOI: https://doi.org/10.1007/s12020-016-0857-1

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