Association between trabecular bone score and type 2 diabetes: a quantitative update of evidence

Abstract

Summary

Patients with type 2 diabetes have an increased risk of fracture despite having a higher areal bone mineral density. This meta-analysis showed that compared with controls, diabetic patients had a lower trabecular bone score (TBS) than non-diabetic individuals, suggesting that TBS can be a useful measurement for the assessment of fracture risk in diabetic patients.

Introduction

The association between type 2 diabetes and trabecular bone score (TBS) has not been clear. The present study sought to answer the specific question of whether patients with type 2 diabetes have a lower TBS than those without diabetes.

Methods

Using electronic and manual search, we identified 12 studies that had examined the association between type 2 diabetes and TBS between 2013 and 2019. These studies involved 35,546 women and 4962 men aged 30 years and older. We extracted the mean and standard deviation of TBS for patients with and without diabetes. The synthesis of effect sizes was done by the random effects meta-analysis model.

Results

Patients with diabetes had significantly lower TBS than those without diabetes, with standardized mean difference being − 0.31 (95% CI, − 0.45 to − 0.16). The difference was greater in women (− 0.50; 95% CI, − 0.69 to − 0.32) than in men (− 0.04; 95% CI, − 0.17 to 0.10). Compared with normal individuals, those with prediabetes had significantly lower TBS (d = − 0.13; 95% CI, − 0.23 to − 0.04; P = 0.005). There was heterogeneity between the studies, with the index of inconsistency (I2) ranging from 92% (in women) to 69.5% (in men).

Conclusion

Patients with type 2 diabetes have a lower TBS than non-diabetic individuals, suggesting that TBS can be a useful measurement for the assessment of fracture risk in diabetic patients.

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References

  1. 1.

    Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA. 288(15):1889–1897

    Article  Google Scholar 

  2. 2.

    Fan Y, Wei F, Lang Y, Liu Y (2016) Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporos Int 27(1):219–228

    CAS  Article  Google Scholar 

  3. 3.

    Wang J, You W, Jing Z, Wang R, Fu Z, Wang Y (2016) Increased risk of vertebral fracture in patients with diabetes: a meta-analysis of cohort studies. Int Orthop 40(6):1299–1307

    Article  Google Scholar 

  4. 4.

    Krueger D, Libber J, Binkley N (2015) Spine trabecular bone score precision, a comparison between GE lunar standard and high-resolution densitometers. J Clin Densitom 18(2):226–232

    Article  Google Scholar 

  5. 5.

    Silva BC, Boutroy S, Zhang C, McMahon DJ, Zhou B, Wang J et al (2013) Trabecular bone score (TBS)--a novel method to evaluate bone microarchitectural texture in patients with primary hyperparathyroidism. J Clin Endocrinol Metab 98(5):1963–1970

    CAS  Article  Google Scholar 

  6. 6.

    Jung JY, Han SH, Hong YS, Park SH, Ju JH, Kang KY (2018) Inflammation on spinal magnetic resonance imaging is associated with poor bone quality in patients with ankylosing spondylitis. Mod Rheumatol:1–7

  7. 7.

    Pothuaud L, Carceller P, Hans D (2008) Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone. 42(4):775–787

    Article  Google Scholar 

  8. 8.

    McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H et al (2015) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res

  9. 9.

    Schousboe JT, Vo T, Taylor BC, Cawthon PM, Schwartz AV, Bauer DC et al (2015) 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

  10. 10.

    Leslie WD, Aubry-Rozier B, Lamy O, Hans D, Manitoba Bone Density P (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98(2):602–609

    CAS  Article  Google Scholar 

  11. 11.

    Bonaccorsi G, Fila E, Messina C, Maietti E, Ulivieri FM, Caudarella R, Greco P, Guglielmi G (2017) Comparison of trabecular bone score and hip structural analysis with FRAX((R)) in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res 29(5):951–957

    Article  Google Scholar 

  12. 12.

    Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25(7):1969–1973

    CAS  Article  Google Scholar 

  13. 13.

    Holloway KL, De Abreu LLF, Hans D, Kotowicz MA, Sajjad MA, Hyde NK et al (2018) Trabecular bone score in men and women with impaired fasting glucose and diabetes. Calcif Tissue Int 102(1):32–40

    CAS  Article  Google Scholar 

  14. 14.

    Iki M, Fujita Y, Kouda K, Yura A, Tachiki T, Tamaki J, Winzenrieth R, Sato Y, Moon JS, Okamoto N, Kurumatani N (2017) Hyperglycemia is associated with increased bone mineral density and decreased trabecular bone score in elderly Japanese men: the Fujiwara-kyo osteoporosis risk in men (FORMEN) study. Bone. 105:18–25

    CAS  Article  Google Scholar 

  15. 15.

    Kim JH, Choi HJ, Ku EJ, Kim KM, Kim SW, Cho NH, Shin CS (2015) Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab 100(2):475–482

    CAS  Article  Google Scholar 

  16. 16.

    Wan X, Wang W, Liu J, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 14:135

    Article  Google Scholar 

  17. 17.

    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    CAS  Article  Google Scholar 

  18. 18.

    Normal ST (1999) Meta-analysis: formulating, evaluating, combining, and reporting. Stat Med 18:321–359

    Article  Google Scholar 

  19. 19.

    The National Research Council (1992). Combining information: statistical issues and opportunities for research. Washington DNAP

    Google Scholar 

  20. 20.

    Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Statist Software 36(3):1–48

    Article  Google Scholar 

  21. 21.

    R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Available from: http://www.R-project.org

    Google Scholar 

  22. 22.

    Cochran WG (1954) The combination of estimates from different experiments. Biometrics. 10:101–129

    Article  Google Scholar 

  23. 23.

    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21(11):1539–1558

    Article  Google Scholar 

  24. 24.

    Sterne JA, Gavaghan D, Egger M (2000) Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 53(11):1119–1129

    CAS  Article  Google Scholar 

  25. 25.

    Bax L, Ikeda N, Fukui N, Yaju Y, Tsuruta H, Moons KG (2009) More than numbers: the power of graphs in meta-analysis. Am J Epidemiol 169(2):249–255

    Article  Google Scholar 

  26. 26.

    Caffarelli C, Giambelluca A, Ghini V, Francolini V, Pitinca MDT, Nuti R, Gonnelli S (2017) In type-2 diabetes subjects trabecular bone score is better associated with carotid intima-media thickness than BMD. Calcif Tissue Int 101(4):404–411

    CAS  Article  Google Scholar 

  27. 27.

    Rianon N, Ambrose CG, Buni M, Watt G, Reyes-Ortiz C, Lee M, McCormick J, Fisher-Hoch S (2018) Trabecular bone score is a valuable addition to bone mineral density for bone quality assessment in older Mexican American women with type 2 diabetes. J Clin Densitom 21(3):355–359

    Article  Google Scholar 

  28. 28.

    Xue Y, Baker AL, Nader S, Orlander P, Sanchez AJ, Kellam J, Rianon NJ, Ambrose CG (2018) Lumbar spine trabecular bone score (TBS) reflects diminished bone quality in patients with diabetes mellitus and oral glucocorticoid therapy. J Clin Densitom 21(2):185–192

    Article  Google Scholar 

  29. 29.

    Zhukouskaya VV, Eller-Vainicher C, Gaudio A, Privitera F, Cairoli E, Ulivieri FM et al (2016) 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 27(1):49–56

    CAS  Article  Google Scholar 

  30. 30.

    Wagner AAK (2017) Trabecular bone score in non-diabetic, prediabetic and type II diabetic subjects (MD thesis). Medical University of Graz. Graz, Austria

  31. 31.

    Ho-Pham LT, Tran B, Do AT, Nguyen TV (2019) Association between type 2 diabetes and trabecular bone score: the Vietnam Osteoporosis Study. Submitted

  32. 32.

    McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H et al (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31(5):940–948

    Article  Google Scholar 

  33. 33.

    Wang H, Ba Y, Xing Q, Du JL (2019) Diabetes mellitus and the risk of fractures at specific sites: a meta-analysis. BMJ Open 9(1):e024067

    Article  Google Scholar 

  34. 34.

    Ho-Pham LT, Chau PMN, Do AT, Nguyen HC, Nguyen TV (2018) Type 2 diabetes is associated with higher trabecular bone density but lower cortical bone density: the Vietnam Osteoporosis Study. Osteoporos Int 29(9):2059–2067

    CAS  Article  Google Scholar 

  35. 35.

    Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM (2010) High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 95(11):5045–5055

    CAS  Article  Google Scholar 

  36. 36.

    Farr JN, Drake MT, Amin S, Melton LJ 3rd, McCready LK, Khosla S (2014) In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res 29(4):787–795

    Article  Google Scholar 

  37. 37.

    Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellstrom D, Rudang R et al (2017) Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population-based study. J Bone Miner Res 32(5):1062–1071

    Article  Google Scholar 

  38. 38.

    Saito M, Fujii K, Mori Y, Marumo K (2006) Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int 17(10):1514–1523

    CAS  Article  Google Scholar 

  39. 39.

    Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer DC, for the Health, Aging, and Body Composition Study (2009) Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 94(7):2380–2386

    CAS  Article  Google Scholar 

  40. 40.

    Choi YJ, Ock SY, Jin Y, Lee JS, Kim SH, Chung Y (2018) Urinary pentosidine levels negatively associates with trabecular bone scores in patients with type 2 diabetes mellitus. Osteoporos Int 29(4):907–915

    CAS  Article  Google Scholar 

  41. 41.

    Napoli N, Schwartz AV, Schafer AL, Vittinghoff E, Cawthon PM, Parimi N, Orwoll E, Strotmeyer ES, Hoffman AR, Barrett-Connor E, Black DM, for the Osteoporotic Fractures in Men (MrOS) Study Research Group (2018) Vertebral fracture risk in diabetic elderly men: the MrOS study. J Bone Miner Res 33(1):63–69

    Article  Google Scholar 

  42. 42.

    Tenne M, McGuigan F, Besjakov J, Gerdhem P, Akesson K (2013) Degenerative changes at the lumbar spine--implications for bone mineral density measurement in elderly women. Osteoporos Int 24(4):1419–1428

    CAS  Article  Google Scholar 

  43. 43.

    Field AP (2001) Meta-analysis of correlation coefficients: a Monte Carlo comparison of fixed- and random-effects methods. Psychol Methods 6(2):161–180

    CAS  Article  Google Scholar 

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Funding

This research is funded by Foundation for Science and Technology Development of Ton Duc Thang University (FOSTECT, http://fostect.tdt.edu.vn), grant number FOSTECT.2014.BR.09, and a grant from the Department of Science and Technology of Ho Chi Minh City.

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Correspondence to L. T. Ho-Pham.

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Ho-Pham, L.T., Nguyen, T.V. Association between trabecular bone score and type 2 diabetes: a quantitative update of evidence. Osteoporos Int 30, 2079–2085 (2019). https://doi.org/10.1007/s00198-019-05053-z

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Keywords

  • Bone mineral density
  • Meta-analysis
  • Trabecular bone score
  • Type 2 diabetes