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Trabecular Bone Score in Men and Women with Impaired Fasting Glucose and Diabetes

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Abstract

Diabetes is associated with increased skeletal fragility, despite higher bone mineral density (BMD). Alternative measures are necessary to more accurately determine fracture risk in individuals with diabetes. Therefore, we aimed to describe the relationship between trabecular bone score (TBS) and normoglycaemia, impaired fasting glucose (IFG) and diabetes and determine whether TBS-adjusted FRAX (Aus) score differed between these groups. This study included 555 men (68.7 ± 12.2 years) and 514 women (62.0 ± 12.0 years), enrolled in the observational Geelong Osteoporosis Study. IFG was considered as fasting plasma glucose (FPG) ≥ 5.5 mmol/L and diabetes as FPG ≥ 7.0 mmol/L, with the use of antihyperglycaemic medication and/or self-report. Using multivariable regression, the relationship between groups and TBS was determined. Men and women (all ages) with diabetes had lower mean TBS compared to those with normoglycaemia, in models adjusted for age, height and weight/waist circumference (all p < 0.05). Men with IFG had lower mean TBS in the age-adjusted models only (all p < 0.05). The addition of TBS to the FRAX score improved the discrimination between glycaemia groups, particularly for younger women (< 65 years). There was no difference in TBS detected between normoglycaemia and IFG; however, those with diabetes had lower TBS. Thus, the increased fracture risk in men and women with diabetes may be a result of BMD-independent bone deterioration. TBS adjustment of FRAX scores may be useful for younger women (< 65 years) with diabetes. This suggests that halting or reversing progression from IFG to diabetes could be important to prevent skeletal fragility in diabetes.

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References

  1. Sealand R, Razavi C, Adler RA (2013) Diabetes mellitus and osteoporosis. Curr Diabetes Rep 13:411–418

    Article  CAS  Google Scholar 

  2. Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TT, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV (2014) Fracture risk in diabetic elderly men: the MrOS study. Diabetologia 57:2057–2065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Shibuya N, Humphers JM, Fluhman BL, Jupiter DC (2013) Factors associated with nonunion, delayed union, and malunion in foot and ankle surgery in diabetic patients. J Foot Ankle Surg 52:207–211

    Article  PubMed  Google Scholar 

  4. Gehling DJ, Lecka-Czernik B, Ebraheim NA (2016) Orthopedic complications in diabetes. Bone 82:79–92

    Article  PubMed  Google Scholar 

  5. Giangregorio LM, Leslie WD, Lix LM, Johansson H, Oden A, McCloskey E, Kanis JA (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 27:301–308

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  7. Harvey NC, Gluer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C, Kendler D, Lamy O, Laslop A, Camargos BM, Reginster JY, Rizzoli R, Kanis JA (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29:518–530

    Article  PubMed  Google Scholar 

  9. Ulivieri FM, Silva BC, Sardanelli F, Hans D, Bilezikian JP, Caudarella R (2014) Utility of the trabecular bone score (TBS) in secondary osteoporosis. Endocrine 47:435–448

    Article  CAS  PubMed  Google Scholar 

  10. Iki M, Fujita Y, Tamaki J, Kouda K, Yura A, Sato Y, Moon J-S, Winzenrieth R, Okamoto N, Kurumatani N (2015) Trabecular bone score may improve FRAX® prediction accuracy for major osteoporotic fractures in elderly Japanese men: the Fujiwara-kyo osteoporosis risk in Men (FORMEN) cohort study. Osteoporos Int 26:1841–1848

    Article  CAS  PubMed  Google Scholar 

  11. Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14:302–312

    Article  PubMed  Google Scholar 

  12. Muschitz C, Kocijan R, Haschka J, Pahr D, Kaider A, Pietschmann P, Hans D, Muschitz GK, Fahrleitner-Pammer A, Resch H (2015) TBS reflects trabecular microarchitecture in premenopausal women and men with idiopathic osteoporosis and low-traumatic fractures. Bone 79:259–266

    Article  PubMed  Google Scholar 

  13. Roux JP, Wegrzyn J, Boutroy S, Bouxsein ML, Hans D, Chapurlat R (2013) The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study. Osteoporos Int 24:2455–2460

    Article  CAS  PubMed  Google Scholar 

  14. McCloskey EV, Odén A, Harvey NC, Leslie WD, Hans D, Johansson H, Kanis JA (2015) Adjusting fracture probability by trabecular bone score. Calcif Tissue Int 96:500–509

    Article  CAS  PubMed  Google Scholar 

  15. Pasco JA, Seeman E, Henry MJ, Merriman EN, Nicholson GC, Kotowicz MA (2006) The population burden of fractures originates in women with osteopenia, not osteoporosis. Osteoporos Int 17:1404–1409

    Article  CAS  PubMed  Google Scholar 

  16. Pasco JA, Lane SE, Brennan SL, Timney EN, Bucki-Smith G, Dobbins AG, Nicholson GC, Kotowicz MA (2014) Fracture risk among older men: osteopenia and osteoporosis defined using cut-points derived from female versus male reference data. Osteoporos Int 25:857–862

    Article  CAS  PubMed  Google Scholar 

  17. Bauer D (2011) FRAX, falls, and fracture prediction: predicting the future. Arch Intern Med 171:1661–1662

    Article  PubMed  Google Scholar 

  18. Leslie WD, Johansson H, Kanis JA, Lamy O, Oden A, McCloskey EV, Hans D (2014) Lumbar spine texture enhances 10-year fracture probability assessment. Osteoporos Int 25:2271–2277

    Article  CAS  PubMed  Google Scholar 

  19. Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J Clin Densitom 18:309–330

    Article  PubMed  Google Scholar 

  20. Neumann T, Lodes S, Kastner B, Lehmann T, Hans D, Lamy O, Muller UA, Wolf G, Samann A (2016) Trabecular bone score in type 1 diabetes–a cross-sectional study. Osteoporos Int 27:127–133

    Article  CAS  PubMed  Google Scholar 

  21. Bonaccorsi G, Fila E, Messina C, Maietti E, Ulivieri FM, Caudarella R, Greco P, Guglielmi G (2016) Comparison of trabecular bone score and hip structural analysis with FRAX(R) in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res. doi:10.1007/s40520-016-0634-2

    PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Zhukouskaya VV, Eller-Vainicher C, Gaudio A, Privitera F, Cairoli E, Ulivieri FM, Palmieri S, Morelli V, Grancini V, Orsi E, Masserini B, Spada AM, Fiore CE, Chiodini I (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 27:49–56

    Article  CAS  PubMed  Google Scholar 

  25. 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 100:475–482

    Article  CAS  PubMed  Google Scholar 

  26. Choi YJ, Ock SY, Chung YS (2016) Trabecular bone score (TBS) and TBS-adjusted fracture risk assessment tool are potential supplementary tools for the discrimination of morphometric vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Densitom 19:507–514

    Article  PubMed  Google Scholar 

  27. Pasco JA, Nicholson GC, Kotowicz MA (2012) Cohort profile: Geelong osteoporosis study. Int J Epidemiol 41:1565–1575

    Article  PubMed  Google Scholar 

  28. Sanders KM, Pasco JA, Ugoni AM, Nicholson GC, Seeman E, Martin TJ, Skoric B, Panahi S, Kotowicz MA (1998) The exclusion of high trauma fractures may underestimate the prevalence of bone fragility fractures in the community: the Geelong osteoporosis study. J Bone Miner Res 13:1337–1342

    Article  CAS  PubMed  Google Scholar 

  29. Giles G, Ireland P (1996) Dietary questionnaire for epidemiological studies (version 2). Melbourne, The Cancer Council Victoria

    Google Scholar 

  30. Brennan S, Quirk S, Hosking S, Kotowicz M, Holloway K, Moloney D, Dobbins A, Pasco JA (2015) Is There an interaction between socioeconomic status and FRAX 10-year fracture probability determined with and without bone density measures? Data from the Geelong osteoporosis study of female cohort. Calcif Tissue Int 96:138–144

    Article  CAS  PubMed  Google Scholar 

  31. Kunst ADB, Ziegenhorn J (1984) UV-methods with hexokinase and glucose-6-phosphate dehydrogenase. Chemie, Weinheim

    Google Scholar 

  32. Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, Kitzmiller J, Knowler WC, Lebovitz H, Lernmark A, Nathan D, Palmer J, Rizza R, Saudek C, Shaw J, Steffes M, Stern M, Tuomilehto J, Zimmet P (2003) Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 26:3160–3167

    Article  PubMed  Google Scholar 

  33. University of Sheffield UK (2011) FRAX® WHO fracture risk assessment tool 2011 [cited August 2017]. Available from: http://www.shef.ac.uk/FRAX/

  34. Romagnoli E, Lubrano C, Carnevale V, Costantini D, Nieddu L, Morano S, Migliaccio S, Gnessi L, Lenzi A (2016) Assessment of trabecular bone score (TBS) in overweight/obese men: effect of metabolic and anthropometric factors. Endocrine 54:342–347

    Article  CAS  PubMed  Google Scholar 

  35. Schwartz AV (2016) Epidemiology of fractures in type 2 diabetes. Bone 82:2–8

    Article  PubMed  Google Scholar 

  36. de Abreu L, Holloway K, Kotowicz M, Pasco J (2015) Dysglycaemia and other predictors for progression or regression from impaired fasting glucose to diabetes or normoglycaemia. J Diabetes Res. doi:10.1155/2015/373762

    PubMed  PubMed Central  Google Scholar 

  37. Looker AC, Eberhardt MS, Saydah SH (2016) Diabetes and fracture risk in older US adults. Bone 82:9–15

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Study was supported by the National Health and Medical Research Council (NHMRC) of Australia (251638, 299831, 628582), the Geelong Regional Medical Foundation, Arthritis Foundation of Australia and Perpetual Trustees. NKH is supported by an Australian Postgraduate Award. KLH is supported by an Alfred Deakin Postdoctoral Research Fellowship. LLFA and MAS are supported by Deakin Postgraduate Scholarships.

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Authors and Affiliations

Authors

Contributions

KLH, MAK and JAP conceived the original plan for the study. DH provided TBS data for the study. KLH and JAP carried out the statistical analysis. KLH, MAK, DH and JAP interpreted the results. KLH wrote the original draft of the manuscript and all other authors provided expertise and advice to produce the final version of the manuscript.

Corresponding author

Correspondence to Kara L. Holloway.

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Conflicts of interest

Kara L. Holloway, Lelia L. F. De Abreu, Didier Hans, Mark A. Kotowicz, Muhammad A. Sajjad, Natalie K. Hyde, and Julie A. Pasco have no conflicts of interest to declare.

Human and Animal Rights and Informed Consent

The study was approved by the Barwon Health Human Research Ethics Committee, and written informed consent was obtained from all participants.

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Holloway, K.L., De Abreu, L.L.F., Hans, D. et al. Trabecular Bone Score in Men and Women with Impaired Fasting Glucose and Diabetes. Calcif Tissue Int 102, 32–40 (2018). https://doi.org/10.1007/s00223-017-0330-z

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  • DOI: https://doi.org/10.1007/s00223-017-0330-z

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