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Imaging of diabetic bone

  • Endocrine Methods and Techniques
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Abstract

Diabetes is an important concern in terms of medical and socioeconomic costs; a high risk for low-trauma fractures has been reported in patients with both type 1 and type 2 diabetes. The mechanism involved in the increased fracture risk from diabetes is highly complex and still not entirely understood; obesity could play an important role: recent evidence suggests that the influence of fat on bone is mainly dependent on the pattern of regional fat deposition and that an increased amount of visceral adipose tissue negatively affects skeletal health.

Correct and timely individuation of people with high fracture risk is critical for both prevention and treatment: Dual-energy X-ray Absorptiometry (currently the “gold standard” for diagnosis of osteoporosis) underestimates fracture risk in diabetic patients and therefore is not sufficient by itself to investigate bone status. This paper is focused on imaging, covering different modalities involved in the evaluation of skeletal deterioration in diabetes, discussing the limitations of conventional methods and exploring the potential of new tools and recent high-resolution techniques, with the intent to provide interesting insight into pathophysiology and fracture risk.

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References

  1. A. Menke, S. Casagrande, L. Geiss, C.C. Cowie, Prevalence of and trends in diabetes among adults in the United States, 1988–2012. JAMA 314(10), 1021–1029 (2015). doi:10.1001/jama.2015.10029

    Article  CAS  PubMed  Google Scholar 

  2. J.P. Boyle, T.J. Thompson, E.W. Gregg, L.E. Barker, D.F. Williamson, Projection of the year 2050 burden of diabetes in the US adult population: dynamic modeling of incidence, mortality, and prediabetes prevalence. Popul. Health Metr. 8, 29 (2010). doi:10.1186/1478-7954-8-29

    Article  PubMed  PubMed Central  Google Scholar 

  3. M. Janghorbani, R.M. Van Dam, W.C. Willett, F.B. Hu, Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am. J. Epidemiol. 166(5), 495–505 (2007). doi:10.1093/aje/kwm106

    Article  PubMed  Google Scholar 

  4. L. Oei, F. Rivadeneira, M.C. Zillikens, E.H. Oei, Diabetes, diabetic complications, and fracture risk. Curr. Osteoporos. Rep. 13(2), 106–115 (2015). doi:10.1007/s11914-015-0260-5

    Article  PubMed  PubMed Central  Google Scholar 

  5. L.M. Giangregorio, W.D. Leslie, L.M. Lix, H. Johansson, A. Oden, E. McCloskey, J.A. Kanis, FRAX underestimates fracture risk in patients with diabetes. J. Bone Miner Res. 27(2), 301–308 (2012). doi:10.1002/jbmr.556

    Article  PubMed  Google Scholar 

  6. A.V. Schwartz, E. Vittinghoff, D.C. Bauer, T.A. Hillier, E.S. Strotmeyer, K.E. Ensrud, M.G. Donaldson, J.A. Cauley, T.B. Harris, A. Koster, C.R. Womack, L. Palermo, D.M. Black, Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305(21), 2184–2192 (2011). doi:10.1001/jama.2011.715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. A.V. Schwartz, D.E. Sellmeyer, Diabetes, fracture, and bone fragility. Curr. Osteoporos. Rep. 5(3), 105–111 (2007)

    Article  PubMed  Google Scholar 

  8. J.F. Griffith, H.K. Genant, New advances in imaging osteoporosis and its complications. Endocrine 42(1), 39–51 (2012). doi:10.1007/s12020-012-9691-2

    Article  CAS  PubMed  Google Scholar 

  9. M.L. Isidro, B. Ruano, Bone disease in diabetes. Curr. Diabetes Rev. 6(3), 144–155 (2010)

    Article  PubMed  Google Scholar 

  10. S. Yamagishi, Role of advanced glycation end products (AGEs) in osteoporosis in diabetes. Curr. Drug Targets 12(14), 2096–2102 (2011)

    Article  CAS  PubMed  Google Scholar 

  11. M. Saito, K. Fujii, S. Soshi, T. Tanaka, Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos. Int. 17(7), 986–995 (2006). doi:10.1007/s00198-006-0087-0

    Article  CAS  PubMed  Google Scholar 

  12. P.E. Witten, A. Huysseune, A comparative view on mechanisms and functions of skeletal remodelling in teleost fish, with special emphasis on osteoclasts and their function. Biol. Rev. Camb. Philos. Soc. 84(2), 315–346 (2009). doi:10.1111/j.1469-185X.2009.00077.x

    Article  PubMed  Google Scholar 

  13. M. Carnovali, L. Luzi, G. Banfi, M. Mariotti, Chronic hyperglycemia affects bone metabolism in adult zebrafish scale model. Endocrine 54(3), 808–817 (2016). doi:10.1007/s12020-016-1106-3

    Article  CAS  PubMed  Google Scholar 

  14. N. Suzuki, K.I. Kitamura, A. Hattori, Fish scale is a suitable model for analyzing determinants of skeletal fragility in type 2 diabetes. Endocrine 54(3), 575–577 (2016). doi:10.1007/s12020-016-1153-9

    Article  CAS  PubMed  Google Scholar 

  15. S. Bermeo, K. Gunaratnam, G. Duque, Fat and bone interactions. Curr. Osteoporos. Rep. 12(2), 235–242 (2014). doi:10.1007/s11914-014-0199-y

    Article  PubMed  Google Scholar 

  16. G. Guglielmi, F. Ponti, M. Agostini, M. Amadori, G. Battista, A. Bazzocchi: The role of DXA in sarcopenia. Aging. Clin. Exp. Res. (2016). doi:10.1007/s40520-016-0589-3

  17. A. Bazzocchi, F. Ponti, S. Cariani, D. Diano, L. Leuratti, U. Albisinni, G. Marchesini, G. Battista, Visceral fat and body composition changes in a female population after RYGBP: a two-year follow-up by DXA. Obes. Surg. 25(3), 443–451 (2015). doi:10.1007/s11695-014-1422-8

    Article  PubMed  Google Scholar 

  18. C. Albala, M. Yanez, E. Devoto, C. Sostin, L. Zeballos, J.L. Santos, Obesity as a protective factor for postmenopausal osteoporosis. Int. J. Obes. Relat. Metab. Disord. 20(11), 1027–1032 (1996)

    CAS  PubMed  Google Scholar 

  19. V. Gilsanz, J. Chalfant, A.O. Mo, D.C. Lee, F.J. Dorey, S.D. Mittelman, Reciprocal relations of subcutaneous and visceral fat to bone structure and strength. J. Clin. Endocrinol. Metab. 94(9), 3387–3393 (2009). doi:10.1210/jc.2008-2422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. A. Cohen, D.W. Dempster, R.R. Recker, J.M. Lappe, H. Zhou, A. Zwahlen, R. Muller, B. Zhao, X. Guo, T. Lang, I. Saeed, X.S. Liu, X.E. Guo, S. Cremers, C.J. Rosen, E.M. Stein, T.L. Nickolas, D.J. McMahon, P. Young, E. Shane, Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J. Clin. Endocrinol. Metab. 98(6), 2562–2572 (2013). doi:10.1210/jc.2013-1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. E.A. Greco, A. Lenzi, S. Migliaccio, The obesity of bone. Ther. Adv. Endocrinol. Metab. 6(6), 273–286 (2015). doi:10.1177/2042018815611004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. C.J. Rosen, M.L. Bouxsein, Mechanisms of disease: is osteoporosis the obesity of bone? Nat. Clin. Pract. Rheumatol. 2(1), 35–43 (2006). doi:10.1038/ncprheum0070

    Article  CAS  PubMed  Google Scholar 

  23. K.O. Klein, K.A. Larmore, E. de Lancey, J.M. Brown, R.V. Considine, S.G. Hassink, Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children. J. Clin. Endocrinol. Metab. 83(10), 3469–3475 (1998). doi:10.1210/jcem.83.10.5204

    Article  CAS  PubMed  Google Scholar 

  24. M. Yamauchi, T. Sugimoto, T. Yamaguchi, D. Nakaoka, M. Kanzawa, S. Yano, R. Ozuru, T. Sugishita, K. Chihara, Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin. Endocrinol. (Oxf). 55(3), 341–347 (2001)

    Article  CAS  PubMed  Google Scholar 

  25. K.M. Pou, J.M. Massaro, U. Hoffmann, R.S. Vasan, P. Maurovich-Horvat, M.G. Larson, J.F. Keaney Jr., J.B. Meigs, I. Lipinska, S. Kathiresan, J.M. Murabito, C.J. O’Donnell, E.J. Benjamin, C.S. Fox, Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham heart study. Circulation 116(11), 1234–1241 (2007). doi:10.1161/circulationaha.107.710509

    Article  CAS  PubMed  Google Scholar 

  26. A. Cartier, I. Lemieux, N. Almeras, A. Tremblay, J. Bergeron, J.P. Despres, Visceral obesity and plasma glucose-insulin homeostasis: contributions of interleukin-6 and tumor necrosis factor-alpha in men. J. Clin. Endocrinol. Metab. 93(5), 1931–1938 (2008). doi:10.1210/jc.2007-2191

    Article  CAS  PubMed  Google Scholar 

  27. F.F. Horber, B. Gruber, F. Thomi, E.X. Jensen, P. Jaeger, Effect of sex and age on bone mass, body composition and fuel metabolism in humans. Nutrition. 13(6), 524–534 (1997)

    Article  CAS  PubMed  Google Scholar 

  28. J.C. Lovejoy, C.M. Champagne, L. de Jonge, H. Xie, S.R. Smith, Increased visceral fat and decreased energy expenditure during the menopausal transition. Int. J. Obes. 32(6), 949–958 (2008). doi:10.1038/ijo.2008.25

    Article  CAS  Google Scholar 

  29. C.J. Rosen, C. Ackert-Bicknell, J.P. Rodriguez, A.M. Pino, Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit. Rev. Eukaryot. Gene Expr. 19(2), 109–124 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. M.A. Bredella, Perspective: the bone-fat connection. Skeletal Radiol. 39(8), 729–731 (2010). doi:10.1007/s00256-010-0936-y

    Article  PubMed  Google Scholar 

  31. S. Adami, Bone health in diabetes: considerations for clinical management. Curr. Med. Res. Opin. 25(5), 1057–1072 (2009). doi:10.1185/03007990902801147

    Article  PubMed  Google Scholar 

  32. M.N. Weitzmann, R. Pacifici, Estrogen deficiency and bone loss: an inflammatory tale. J. Clin. Invest. 116(5), 1186–1194 (2006). doi:10.1172/jci28550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. B. Lecka-Czernik, C. Ackert-Bicknell, M.L. Adamo, V. Marmolejos, G.A. Churchill, K.R. Shockley, I.R. Reid, A. Grey, C.J. Rosen, Activation of peroxisome proliferator-activated receptor gamma (PPARgamma) by rosiglitazone suppresses components of the insulin-like growth factor regulatory system in vitro and in vivo. Endocrinology 148(2), 903–911 (2007). doi:10.1210/en.2006-1121

    Article  CAS  PubMed  Google Scholar 

  34. Y. Jiang, B.N. Jahagirdar, R.L. Reinhardt, R.E. Schwartz, C.D. Keene, X.R. Ortiz-Gonzalez, M. Reyes, T. Lenvik, T. Lund, M. Blackstad, J. Du, S. Aldrich, A. Lisberg, W.C. Low, D.A. Largaespada, C.M. Verfaillie, Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418(6893), 41–49 (2002). doi:10.1038/nature00870

    Article  CAS  PubMed  Google Scholar 

  35. P.K. Fazeli, M.C. Horowitz, O.A. MacDougald, E.L. Scheller, M.S. Rodeheffer, C.J. Rosen, A. Klibanski, Marrow fat and bone--new perspectives. J. Clin. Endocrinol. Metab. 98(3), 935–945 (2013). doi:10.1210/jc.2012-3634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. J.J. Minguell, A. Erices, P. Conget, Mesenchymal stem cells. Exp. Biol. Med. (Maywood) 226(6), 507–520 (2001)

    Article  CAS  Google Scholar 

  37. S. Verma, J.H. Rajaratnam, J. Denton, J.A. Hoyland, R.J. Byers, Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J. Clin. Pathol. 55(9), 693–698 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. S. Kang, C.N. Bennett, I. Gerin, L.A. Rapp, K.D. Hankenson, O.A. Macdougald, Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J. Biol. Chem. 282(19), 14515–14524 (2007). doi:10.1074/jbc.M700030200

    Article  CAS  PubMed  Google Scholar 

  39. J.M. Gimble, S. Zvonic, Z.E. Floyd, M. Kassem, M.E. Nuttall, Playing with bone and fat. J. Cell. Biochem. 98(2), 251–266 (2006). doi:10.1002/jcb.20777

    Article  CAS  PubMed  Google Scholar 

  40. A. Elbaz, X. Wu, D. Rivas, J.M. Gimble, G. Duque, Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro. J. Cell. Mol. Med. 14(4), 982–991 (2010). doi:10.1111/j.1582-4934.2009.00751.x

    Article  CAS  PubMed  Google Scholar 

  41. A.C. Maurin, P.M. Chavassieux, L. Frappart, P.D. Delmas, C.M. Serre, P.J. Meunier, Influence of mature adipocytes on osteoblast proliferation in human primary cocultures. Bone 26(5), 485–489 (2000). doi:10.1016/s8756-3282(00)00252-0

    Article  CAS  PubMed  Google Scholar 

  42. K. Gunaratnam, C. Vidal, J.M. Gimble, G. Duque, Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology 155(1), 108–116 (2014). doi:10.1210/en.2013-1712

    Article  PubMed  CAS  Google Scholar 

  43. S. Muruganandan, C.J. Sinal: The impact of bone marrow adipocytes on osteoblast and osteoclast differentiation. IUBMB Life (2014). doi:10.1002/iub.1254

  44. Y. Liu, C.Y. Song, S.S. Wu, Q.H. Liang, L.Q. Yuan, E.Y. Liao, Novel adipokines and bone metabolism. Int. J. Endocrinol. 2013, 895045 (2013). doi:10.1155/2013/895045

    PubMed  PubMed Central  Google Scholar 

  45. M.E. Arlot, Y. Jiang, H.K. Genant, J. Zhao, B. Burt-Pichat, J.P. Roux, P.D. Delmas, P.J. Meunier, Histomorphometric and microCT analysis of bone biopsies from postmenopausal osteoporotic women treated with strontium ranelate. J. Bone Miner Res. 23(2), 215–222 (2008). doi:10.1359/jbmr.071012

    Article  CAS  PubMed  Google Scholar 

  46. F. Rauch, Watching bone cells at work: what we can see from bone biopsies. Pediatr. Nephrol. 21(4), 457–462 (2006). doi:10.1007/s00467-006-0025-6

    Article  PubMed  Google Scholar 

  47. B. Vidal, A. Pinto, M.J. Galvao, A.R. Santos, A. Rodrigues, R. Cascao, S. Abdulghani, J. Caetano-Lopes, A. Ferreira, J.E. Fonseca, H. Canhao, Bone histomorphometry revisited. Acta Reumatol. Port. 37(4), 294–300 (2012)

    CAS  PubMed  Google Scholar 

  48. A.M. Parfitt, M.K. Drezner, F.H. Glorieux, J.A. Kanis, H. Malluche, P.J. Meunier, S.M. Ott, R.R. Recker, Bone histomorphometry: standardization of nomenclature, symbols, and units: report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2(6), 595–610 (1987). doi:10.1002/jbmr.5650020617

    Article  CAS  PubMed  Google Scholar 

  49. M.E. Leite Duarte, R.D. da Silva, [Histomorphometric analysis of the bone tissue in patients with non-insulin-dependent diabetes (DMNID)]. Rev. Hosp. Clin. Fac. Med. Sao Paulo 51(1), 7–11 (1996)

    CAS  PubMed  Google Scholar 

  50. C.A. Moreira, D.W. Dempster, Bone histomorphometry in diabetes mellitus. Osteoporos. Int. 26(11), 2559–2560 (2015). doi:10.1007/s00198-015-3258-z

    Article  CAS  PubMed  Google Scholar 

  51. J.S. Manavalan, S. Cremers, D.W. Dempster, H. Zhou, E. Dworakowski, A. Kode, S. Kousteni, M.R. Rubin, Circulating osteogenic precursor cells in type 2 diabetes mellitus. J. Clin. Endocrinol. Metab 97(9), 3240–3250 (2012). doi:10.1210/jc.2012-1546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. A. Cohen, D.W. Dempster, R. Muller, X.E. Guo, T.L. Nickolas, X.S. Liu, X.H. Zhang, A.J. Wirth, G.H. van Lenthe, T. Kohler, D.J. McMahon, H. Zhou, M.R. Rubin, J.P. Bilezikian, J.M. Lappe, R.R. Recker, E. Shane, Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos. Int. 21(2), 263–273 (2010). doi:10.1007/s00198-009-0945-7

    Article  CAS  PubMed  Google Scholar 

  53. J.A. MacNeil, S.K. Boyd, Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med. Eng. Phys. 29(10), 1096–1105 (2007). doi:10.1016/j.medengphy.2006.11.002

    Article  PubMed  Google Scholar 

  54. L.A. Armas, M.P. Akhter, A. Drincic, R.R. Recker, Trabecular bone histomorphometry in humans with Type 1 Diabetes Mellitus. Bone 50(1), 91–96 (2012). doi:10.1016/j.bone.2011.09.055

    Article  PubMed  Google Scholar 

  55. P. Vestergaard, Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos. Int. 18(4), 427–444 (2007). doi:10.1007/s00198-006-0253-4

    Article  CAS  PubMed  Google Scholar 

  56. D.E. Bonds, J.C. Larson, A.V. Schwartz, E.S. Strotmeyer, J. Robbins, B.L. Rodriguez, K.C. Johnson, K.L. Margolis, Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J. Clin. Endocrinol. Metab. 91(9), 3404–3410 (2006). doi:10.1210/jc.2006-0614

    Article  CAS  PubMed  Google Scholar 

  57. P. Vestergaard, L. Rejnmark, L. Mosekilde, Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48(7), 1292–1299 (2005). doi:10.1007/s00125-005-1786-3

    Article  CAS  PubMed  Google Scholar 

  58. K.K. Nicodemus, A.R. Folsom, Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24(7), 1192–1197 (2001)

    Article  CAS  PubMed  Google Scholar 

  59. D.R. Weber, K. Haynes, M.B. Leonard, S.M. Willi, M.R. Denburg, Type 1 diabetes is associated with an increased risk of fracture across the life span: a population-based cohort study using The Health Improvement Network (THIN). Diabetes Care 38(10), 1913–1920 (2015). doi:10.2337/dc15-0783

    Article  PubMed  PubMed Central  Google Scholar 

  60. A.C. Looker, M.S. Eberhardt, S.H. Saydah, Diabetes and fracture risk in older U.S. adults. Bone 82, 9–15 (2016). doi:10.1016/j.bone.2014.12.008

    Article  PubMed  Google Scholar 

  61. V.V. Zhukouskaya, C. Eller-Vainicher, V.V. Vadzianava, A.P. Shepelkevich, I.V. Zhurava, G.G. Korolenko, O.B. Salko, E. Cairoli, P. Beck-Peccoz, I. Chiodini, Prevalence of morphometric vertebral fractures in patients with type 1 diabetes. Diabetes Care 36(6), 1635–1640 (2013). doi:10.2337/dc12-1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. J. Dytfeld, M. Michalak: Type 2 diabetes and risk of low-energy fractures in postmenopausal women: meta-analysis of observational studies. Aging Clin. Exp. Res. (2016). doi:10.1007/s40520-016-0562-1

  63. D.A. Hanley, J.P. Brown, A. Tenenhouse, W.P. Olszynski, G. Ioannidis, C. Berger, J.C. Prior, L. Pickard, T.M. Murray, T. Anastassiades, S. Kirkland, C. Joyce, L. Joseph, A. Papaioannou, S.A. Jackson, S. Poliquin, J.D. Adachi, Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J. Bone Miner. Res. 18(4), 784–790 (2003). doi:10.1359/jbmr.2003.18.4.784

    Article  CAS  PubMed  Google Scholar 

  64. M. Yamamoto, T. Yamaguchi, M. Yamauchi, H. Kaji, T. Sugimoto, Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J. Bone Miner. Res. 24(4), 702–709 (2009). doi:10.1359/jbmr.081207

    Article  CAS  PubMed  Google Scholar 

  65. C. Cooper, E.J. Atkinson, W.M. O’Fallon, L.J. Melton 3rd, Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985-1989. J. Bone Miner. Res. 7(2), 221–227 (1992). doi:10.1002/jbmr.5650070214

    Article  CAS  PubMed  Google Scholar 

  66. C.M. Klotzbuecher, P.D. Ross, P.B. Landsman, T.A. Abbott 3rd, M. Berger, Patients with prior fractures have an increased risk of future fractures: a summary of the literature and statistical synthesis. J. Bone Miner. Res. 15(4), 721–739 (2000). doi:10.1359/jbmr.2000.15.4.721

    Article  CAS  PubMed  Google Scholar 

  67. A. Bazzocchi, G. Guglielmi, Vertebral fracture identification. Semin. Musculoskelet. Radiol. 20(4), 317–329 (2016). doi:10.1055/s-0036-1592435

    Article  PubMed  Google Scholar 

  68. T. Vokes, B. Lentle, The ISCD and vertebral fractures. J. Clin. Densitom. 19(1), 5–7 (2016). doi:10.1016/j.jocd.2014.11.004

    Article  PubMed  Google Scholar 

  69. J. Hawkinson, J. Timins, D. Angelo, M. Shaw, R. Takata, F. Harshaw, Technical white paper: bone densitometry. J. Am Coll Radiol 4(5), 320–327 (2007). doi:10.1016/j.jacr.2007.01.021

    Article  PubMed  Google Scholar 

  70. W.A. Kalender, Effective dose values in bone mineral measurements by photon absorptiometry and computed tomography. Osteoporos. Int. 2(2), 82–87 (1992)

    Article  CAS  PubMed  Google Scholar 

  71. B.F. Wall, D. Hart, Revised radiation doses for typical X-ray examinations. Report on a recent review of doses to patients from medical X-ray examinations in the UK by NRPB. National Radiological Protection Board. Br. J. Radiol. 70(833), 437–439 (1997). doi:10.1259/bjr.70.833.9227222

    Article  CAS  PubMed  Google Scholar 

  72. E. Barnett, B.E. Nordin, The radiological diagnosis of osteoporosis: a new approach. Clin. Radiol. 11, 166–174 (1960)

    Article  CAS  PubMed  Google Scholar 

  73. G. Guglielmi, D. Diacinti, C. van Kuijk, F. Aparisi, C. Krestan, J.E. Adams, T.M. Link, Vertebral morphometry: current methods and recent advances. Eur. Radiol. 18(7), 1484–1496 (2008). doi:10.1007/s00330-008-0899-8

    Article  CAS  PubMed  Google Scholar 

  74. H.K. Genant, C.Y. Wu, C. van Kuijk, M.C. Nevitt, Vertebral fracture assessment using a semiquantitative technique. J. Bone Miner. Res. 8(9), 1137–1148 (1993). doi:10.1002/jbmr.5650080915

    Article  CAS  PubMed  Google Scholar 

  75. J.A. Kanis, N. Burlet, C. Cooper, P.D. Delmas, J.Y. Reginster, F. Borgstrom, R. Rizzoli, European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos. Int. 19(4), 399–428 (2008). doi:10.1007/s00198-008-0560-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Development Committee of the National Osteoporosis Foundation. Osteoporos. Int. 8(4), S1–S2 (1998). doi:10.1007/pl00020934

    Article  Google Scholar 

  77. L. Ferrar, G. Jiang, J. Adams, R. Eastell, Identification of vertebral fractures: an update. Osteoporos. Int. 16(7), 717–728 (2005). doi:10.1007/s00198-005-1880-x

    Article  CAS  PubMed  Google Scholar 

  78. L. Oei, F. Rivadeneira, F. Ly, S.J. Breda, M.C. Zillikens, A. Hofman, A.G. Uitterlinden, G.P. Krestin, E.H. Oei, Review of radiological scoring methods of osteoporotic vertebral fractures for clinical and research settings. Eur. Radiol. 23(2), 476–486 (2013). doi:10.1007/s00330-012-2622-z

    Article  PubMed  Google Scholar 

  79. G.G. Crans, H.K. Genant, J.H. Krege, Prognostic utility of a semiquantitative spinal deformity index. Bone 37(2), 175–179 (2005). doi:10.1016/j.bone.2005.04.003

    Article  PubMed  Google Scholar 

  80. C. Di Somma, M. Rubino, A. Faggiano, L. Vuolo, P. Contaldi, N. Tafuri, M. Andretti, S. Savastano, A. Colao, Spinal deformity index in patients with type 2 diabetes. Endocrine 43(3), 651–658 (2013). doi:10.1007/s12020-012-9848-z

    Article  PubMed  CAS  Google Scholar 

  81. WHO, Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: report of a WHO Study Group. World Health Organ. Tech. Rep. Ser. 843, 1–129 (1994)

    Google Scholar 

  82. A. Bazzocchi, F. Ponti, U. Albisinni, G. Battista, G. Guglielmi, DXA: technical aspects and application. Eur. J. Radiol. 85(8), 1481–1492 (2016). doi:10.1016/j.ejrad.2016.04.004

    Article  PubMed  Google Scholar 

  83. G. Guglielmi, J. Damilakis, G. Solomou, A. Bazzocchi, Quality assurance of imaging techniques used in the clinical management of osteoporosis. Radiol. Med. 117(8), 1347–1354 (2012). doi:10.1007/s11547-012-0881-z

    Article  CAS  PubMed  Google Scholar 

  84. A. Bazzocchi, F. Ciccarese, D. Diano, P. Spinnato, U. Albisinni, C. Rossi, G. Guglielmi, Dual-energy X-ray absorptiometry in the evaluation of abdominal aortic calcifications. J. Clin. Densitom. 15(2), 198–204 (2012). doi:10.1016/j.jocd.2011.11.002

    Article  PubMed  Google Scholar 

  85. L. Oei, M.C. Zillikens, A. Dehghan, G.H. Buitendijk, M.C. Castano-Betancourt, K. Estrada, L. Stolk, E.H. Oei, J.B. van Meurs, J.A. Janssen, A. Hofman, J.P. van Leeuwen, J.C. Witteman, H.A. Pols, A.G. Uitterlinden, C.C. Klaver, O.H. Franco, F. Rivadeneira, High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care 36(6), 1619–1628 (2013). doi:10.2337/dc12-1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. A. Saller, S. Maggi, G. Romanato, P. Tonin, G. Crepaldi, Diabetes and osteoporosis. Aging Clin. Exp. Res. 20(4), 280–289 (2008)

    Article  PubMed  Google Scholar 

  87. J.T. Tuominen, O. Impivaara, P. Puukka, T. Ronnemaa, Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22(7), 1196–1200 (1999)

    Article  CAS  PubMed  Google Scholar 

  88. P.L. van Daele, R.P. Stolk, H. Burger, D. Algra, D.E. Grobbee, A. Hofman, J.C. Birkenhager, H.A. Pols, Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam Study. Ann. Intern. Med. 122(6), 409–414 (1995)

    Article  PubMed  Google Scholar 

  89. S. Yaturu, S. Humphrey, C. Landry, S.K. Jain, Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med. Sci. Monit. 15(1), Cr5–Cr9 (2009)

    PubMed  Google Scholar 

  90. L. Ma, L. Oei, L. Jiang, K. Estrada, H. Chen, Z. Wang, Q. Yu, M.C. Zillikens, X. Gao, F. Rivadeneira, Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur. J. Epidemiol. 27(5), 319–332 (2012). doi:10.1007/s10654-012-9674-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. M.J. Ornstrup, T.N. Kjaer, T. Harslof, H. Stodkilde-Jorgensen, D.M. Hougaard, A. Cohen, S.B. Pedersen, B.L. Langdahl, Adipose tissue, estradiol levels, and bone health in obese men with metabolic syndrome. Eur. J. Endocrinol. 172(2), 205–216 (2015). doi:10.1530/eje-14-0792

    Article  PubMed  CAS  Google Scholar 

  92. L. de II, M. van der Klift, C.E. de Laet, P.L. van Daele, A. Hofman, H.A. Pols, Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos. Int. 16(12), 1713–1720 (2005). doi:10.1007/s00198-005-1909-1

    Article  Google Scholar 

  93. L.D. Hordon, M. Raisi, J.E. Aaron, S.K. Paxton, M. Beneton, J.A. Kanis, : Trabecular architecture in women and men of similar bone mass with and without vertebral fracture: I. Two-dimensional histology. Bone 27(2), 271–276 (2000)

    Article  CAS  PubMed  Google Scholar 

  94. O. Johnell, J.A. Kanis, A. Oden, H. Johansson, C. De Laet, P. Delmas, J.A. Eisman, S. Fujiwara, H. Kroger, D. Mellstrom, P.J. Meunier, L.J. Melton 3rd, T. O’Neill, H. Pols, J. Reeve, A. Silman, A. Tenenhouse, Predictive value of BMD for hip and other fractures. J. Bone Miner. Res. 20(7), 1185–1194 (2005). doi:10.1359/jbmr.050304

    Article  PubMed  Google Scholar 

  95. A. Bazzocchi, F. Fuzzi, G. Garzillo, D. Diano, E. Rimondi, B. Merlino, A. Moio, U. Albisinni, G. Battista, G. Guglielmi, Reliability and accuracy of scout CT in the detection of vertebral fractures. Br. J. Radiol. 86(1032), 20130373 (2013). doi:10.1259/bjr.20130373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. A. Bazzocchi, P. Spinnato, F. Fuzzi, D. Diano, A.M. Morselli-Labate, C. Sassi, E. Salizzoni, G. Battista, G. Guglielmi, Vertebral fracture assessment by new dual-energy X-ray absorptiometry. Bone 50(4), 836–841 (2012). doi:10.1016/j.bone.2012.01.018

    Article  PubMed  Google Scholar 

  97. P. Jackuliak, J. Payer, Osteoporosis, fractures, and diabetes. Int. J. Endocrinol. 2014, 820615 (2014). doi:10.1155/2014/820615

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. M. Saito, K. Fujii, Y. Mori, K. Marumo, 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 (2006). doi:10.1007/s00198-006-0155-5

    Article  CAS  PubMed  Google Scholar 

  99. S.B. Broy, J.A. Cauley, M.E. Lewiecki, J.T. Schousboe, J.A. Shepherd, W.D. Leslie, Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 1: hip geometry. J. Clin. Densitom. 18(3), 287–308 (2015). doi:10.1016/j.jocd.2015.06.005

    Article  PubMed  Google Scholar 

  100. L. Pothuaud, P. Carceller, D. Hans, 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 (2008). doi:10.1016/j.bone.2007.11.018

    Article  PubMed  Google Scholar 

  101. 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 noninvasive analytical method based upon the DXA image. J. Bone Miner. Res. 29(3), 518–530 (2014). doi:10.1002/jbmr.2176

    Article  PubMed  Google Scholar 

  102. N.C. Harvey, C.C. Gluer, 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). doi:10.1016/j.bone.2015.05.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. A. Bazzocchi, F. Ponti, D. Diano, M. Amadori, U. Albisinni, G. Battista, G. Guglielmi, Trabecular bone score in healthy ageing. Br. J. Radiol. 88(1052), 20140865 (2015). doi:10.1259/bjr.20140865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. D. Hans, A.L. Goertzen, M.A. Krieg, W.D. Leslie, Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J. Bone Miner. Res. 26(11), 2762–2769 (2011). doi:10.1002/jbmr.499

    Article  PubMed  Google Scholar 

  105. C. Cormier, O. L, S. Poriau. TBS in routine clinial practice: proposal. (Medimaps Group, Plan‐les‐Outes, 2012)

    Google Scholar 

  106. 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(2), 435–448 (2014). doi:10.1007/s12020-014-0280-4

    Article  CAS  PubMed  Google Scholar 

  107. W.D. Leslie, B. Aubry-Rozier, O. Lamy, D. Hans, TBS (trabecular bone score) and diabetes-related fracture risk. J. Clin. Endocrinol. Metab. 98(2), 602–609 (2013). doi:10.1210/jc.2012-3118

    Article  CAS  PubMed  Google Scholar 

  108. E. Romagnoli, C. Lubrano, V. Carnevale, D. Costantini, L. Nieddu, S. Morano, S. Migliaccio, L. Gnessi, A. Lenzi, Assessment of trabecular bone score (TBS) in overweight/obese men: effect of metabolic and anthropometric factors. Endocrine 54(2), 342–347 (2016). doi:10.1007/s12020-016-0857-1

    Article  CAS  PubMed  Google Scholar 

  109. R. Dhaliwal, D. Cibula, C. Ghosh, R.S. Weinstock, A.M. Moses, Bone quality assessment in type 2 diabetes mellitus. Osteoporos. Int. 25(7), 1969–1973 (2014). doi:10.1007/s00198-014-2704-7

    Article  CAS  PubMed  Google Scholar 

  110. 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(2), 475–482 (2015). doi:10.1210/jc.2014-2047

    Article  CAS  PubMed  Google Scholar 

  111. T. Neumann, S. Lodes, B. Kastner, T. Lehmann, D. Hans, O. Lamy, U.A. Muller, G. Wolf, A. Samann, Trabecular bone score in type 1 diabetes-a cross-sectional study. Osteoporos. Int. 27(1), 127–133 (2016). doi:10.1007/s00198-015-3222-y

    Article  CAS  PubMed  Google Scholar 

  112. T.J. Beck, Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr. Osteoporos. Rep. 5(2), 49–55 (2007)

    Article  PubMed  Google Scholar 

  113. S.L. Bonnick, HSA: beyond BMD with DXA. Bone 41(1 Suppl 1), S9–S12 (2007). doi:10.1016/j.bone.2007.03.007

    PubMed  Google Scholar 

  114. R. Garg, Z. Chen, T. Beck, J.A. Cauley, G. Wu, D. Nelson, B. Lewis, A. LaCroix, M.S. LeBoff, Hip geometry in diabetic women: implications for fracture risk. Metabolism 61(12), 1756–1762 (2012). doi:10.1016/j.metabol.2012.05.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. M. Schorr, L.E. Dichtel, A.V. Gerweck, M. Torriani, K.K. Miller, M.A. Bredella: Body composition predictors of skeletal integrity in obesity. Skeletal Radiol. (2016). doi:10.1007/s00256-016-2363-1

  116. R. Krug, A.J. Burghardt, S. Majumdar, T.M. Link, High-resolution imaging techniques for the assessment of osteoporosis. Radiol. Clin. North Am. 48(3), 601–621 (2010). doi:10.1016/j.rcl.2010.02.015

    Article  PubMed  PubMed Central  Google Scholar 

  117. A.S. Issever, T.M. Link, M. Kentenich, P. Rogalla, A.J. Burghardt, G.J. Kazakia, S. Majumdar, G. Diederichs, Assessment of trabecular bone structure using MDCT: comparison of 64- and 320-slice CT using HR-pQCT as the reference standard. Eur. Radiol. 20(2), 458–468 (2010). doi:10.1007/s00330-009-1571-7

    Article  PubMed  Google Scholar 

  118. W. Tjong, G.J. Kazakia, A.J. Burghardt, S. Majumdar, The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med. Phys. 39(4), 1893–1903 (2012). doi:10.1118/1.3689813

    Article  PubMed  PubMed Central  Google Scholar 

  119. X.S. Liu, X.H. Zhang, K.K. Sekhon, M.F. Adams, D.J. McMahon, J.P. Bilezikian, E. Shane, X.E. Guo, High-resolution peripheral quantitative computed tomography can assess microstructural and mechanical properties of human distal tibial bone. J. Bone Miner. Res. 25(4), 746–756 (2010). doi:10.1359/jbmr.090822

    CAS  PubMed  Google Scholar 

  120. X.S. Liu, A. Cohen, E. Shane, P.T. Yin, E.M. Stein, H. Rogers, S.L. Kokolus, D.J. McMahon, J.M. Lappe, R.R. Recker, T. Lang, X.E. Guo, Bone density, geometry, microstructure, and stiffness: Relationships between peripheral and central skeletal sites assessed by DXA, HR-pQCT, and cQCT in premenopausal women. J. Bone Miner. Res. 25(10), 2229–2238 (2010). doi:10.1002/jbmr.111

    Article  PubMed  PubMed Central  Google Scholar 

  121. A.J. Burghardt, A.S. Issever, A.V. Schwartz, K.A. Davis, U. Masharani, S. Majumdar, T.M. Link, : 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 (2010). doi:10.1210/jc.2010-0226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. J.A. MacNeil, S.K. Boyd, Load distribution and the predictive power of morphological indices in the distal radius and tibia by high resolution peripheral quantitative computed tomography. Bone 41(1), 129–137 (2007). doi:10.1016/j.bone.2007.02.029

    Article  PubMed  Google Scholar 

  123. A.J. Burghardt, G.J. Kazakia, S. Ramachandran, T.M. Link, S. Majumdar, Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J. Bone Miner. Res. 25(5), 983–993 (2010). doi:10.1359/jbmr.091104

    PubMed  Google Scholar 

  124. J.M. Patsch, A.J. Burghardt, S.P. Yap, T. Baum, A.V. Schwartz, G.B. Joseph, T.M. Link, Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J. Bone Miner. Res. 28(2), 313–324 (2013). doi:10.1002/jbmr.1763

    Article  PubMed  PubMed Central  Google Scholar 

  125. V.V. Shanbhogue, S. Hansen, M. Frost, N.R. Jorgensen, A.P. Hermann, J.E. Henriksen, K. Brixen, Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with type 1 diabetes mellitus. J. Bone Miner. Res. 30(12), 2188–2199 (2015). doi:10.1002/jbmr.2573

    Article  CAS  PubMed  Google Scholar 

  126. M. Rix, H. Andreassen, P. Eskildsen, Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22(5), 827–831 (1999)

    Article  CAS  PubMed  Google Scholar 

  127. R. Krug, J. Carballido-Gamio, S. Banerjee, A.J. Burghardt, T.M. Link, S. Majumdar, In vivo ultra-high-field magnetic resonance imaging of trabecular bone microarchitecture at 7 T. J. Magn. Reson. Imaging 27(4), 854–859 (2008). doi:10.1002/jmri.21325

    Article  PubMed  Google Scholar 

  128. F.W. Wehrli, P.K. Saha, B.R. Gomberg, H.K. Song, P.J. Snyder, M. Benito, A. Wright, R. Weening, Role of magnetic resonance for assessing structure and function of trabecular bone. Top Magn. Reson. Imaging 13(5), 335–355 (2002)

    Article  PubMed  Google Scholar 

  129. F.W. Wehrli, B.R. Gomberg, P.K. Saha, H.K. Song, S.N. Hwang, P.J. Snyder, Digital topological analysis of in vivo magnetic resonance microimages of trabecular bone reveals structural implications of osteoporosis. J. Bone Miner. Res. 16(8), 1520–1531 (2001). doi:10.1359/jbmr.2001.16.8.1520

    Article  CAS  PubMed  Google Scholar 

  130. N. Abdalrahaman, C. McComb, J.E. Foster, J. McLean, R.S. Lindsay, J. McClure, M. McMillan, R. Drummond, D. Gordon, G.A. McKay, M.G. Shaikh, C.G. Perry, S.F. Ahmed, Deficits in trabecular bone microarchitecture in young women with type 1 diabetes mellitus. J. Bone Miner. Res. 30(8), 1386–1393 (2015). doi:10.1002/jbmr.2465

    Article  CAS  PubMed  Google Scholar 

  131. J.M. Pritchard, L.M. Giangregorio, S.A. Atkinson, K.A. Beattie, D. Inglis, G. Ioannidis, Z. Punthakee, J.D. Adachi, A. Papaioannou, Association of larger holes in the trabecular bone at the distal radius in postmenopausal women with type 2 diabetes mellitus compared to controls. Arthritis Care Res. 64(1), 83–91 (2012). doi:10.1002/acr.20602

    Article  Google Scholar 

  132. D. Schellinger, C.S. Lin, J. Lim, H.G. Hatipoglu, J.C. Pezzullo, A.J. Singer, Bone marrow fat and bone mineral density on proton MR spectroscopy and dual-energy X-ray absorptiometry: their ratio as a new indicator of bone weakening. Am. J. Roentgenol. 183(6), 1761–1765 (2004). doi:10.2214/ajr.183.6.01831761

    Article  CAS  Google Scholar 

  133. D. Schellinger, C.S. Lin, H.G. Hatipoglu, D. Fertikh, Potential value of vertebral proton MR spectroscopy in determining bone weakness. Am. J. Neuroradiol. 22(8), 1620–1627 (2001)

    CAS  PubMed  Google Scholar 

  134. J.B. Vogler 3rd, W.A. Murphy, Bone marrow imaging. Radiology 168(3), 679–693 (1988). doi:10.1148/radiology.168.3.3043546

    Article  PubMed  Google Scholar 

  135. D.K. Yeung, J.F. Griffith, G.E. Antonio, F.K. Lee, J. Woo, P.C. Leung, Osteoporosis is associated with increased marrow fat content and decreased marrow fat unsaturation: a proton MR spectroscopy study. J. Magn. Reson. Imaging 22(2), 279–285 (2005). doi:10.1002/jmri.20367

    Article  PubMed  Google Scholar 

  136. T. Baum, S.P. Yap, D.C. Karampinos, L. Nardo, D. Kuo, A.J. Burghardt, U.B. Masharani, A.V. Schwartz, X. Li, T.M. Link, Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine bone mineral density, and blood biomarkers in women with type 2 diabetes mellitus? J. Magn. Reson. Imaging 35(1), 117–124 (2012). doi:10.1002/jmri.22757

    Article  PubMed  Google Scholar 

  137. E.W. Yu, L. Greenblatt, A. Eajazi, M. Torriani, M.A. Bredella, Marrow adipose tissue composition in adults with morbid obesity. Bone 97, 38–42 (2017). doi:10.1016/j.bone.2016.12.018

    Article  CAS  PubMed  Google Scholar 

  138. J.M. Patsch, X. Li, T. Baum, S.P. Yap, D.C. Karampinos, A.V. Schwartz, T.M. Link, Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J. Bone Miner. Res. 28(8), 1721–1728 (2013). doi:10.1002/jbmr.1950

    Article  PubMed  PubMed Central  Google Scholar 

  139. J.M. Slade, L.M. Coe, R.A. Meyer, L.R. McCabe, Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes. J. Diabetes Complicat. 26(1), 1–9 (2012). doi:10.1016/j.jdiacomp.2011.11.001

    Article  PubMed  Google Scholar 

  140. A.B. Longo, W.E. Ward, PUFAs, bone mineral density, and fragility fracture: findings from human studies. Adv. Nutr. 7(2), 299–312 (2016). doi:10.3945/an.115.009472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. T.S. Orchard, J.A. Cauley, G.C. Frank, M.L. Neuhouser, J.G. Robinson, L. Snetselaar, F. Tylavsky, J. Wactawski-Wende, A.M. Young, B. Lu, R.D. Jackson, Fatty acid consumption and risk of fracture in the Women’s health initiative. Am. J. Clin. Nutr. 92(6), 1452–1460 (2010). doi:10.3945/ajcn.2010.29955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. C.C. Gluer, Quantitative ultrasound techniques for the assessment of osteoporosis: expert agreement on current status. The International Quantitative Ultrasound Consensus Group. J. Bone Miner. Res. 12(8), 1280–1288 (1997). doi:10.1359/jbmr.1997.12.8.1280

    Article  CAS  PubMed  Google Scholar 

  143. D. Hans, C.F. Njeh, H.K. Genant, P.J. Meunier, Quantitative ultrasound in bone status assessment. Rev. Rhum. Engl. Ed. 65(7–9), 489–498 (1998)

    CAS  PubMed  Google Scholar 

  144. G. Guglielmi, G. Scalzo, F. de Terlizzi, W.C. Peh, Quantitative ultrasound in osteoporosis and bone metabolism pathologies. Radiol. Clin. North Am. 48(3), 577–588 (2010). doi:10.1016/j.rcl.2010.02.013

    Article  PubMed  Google Scholar 

  145. D. Hans, P. Dargent-Molina, A.M. Schott, J.L. Sebert, C. Cormier, P.O. Kotzki, P.D. Delmas, J.M. Pouilles, G. Breart, P.J. Meunier, Ultrasonographic heel measurements to predict hip fracture in elderly women: the EPIDOS prospective study. Lancet 348(9026), 511–514 (1996)

    Article  CAS  PubMed  Google Scholar 

  146. G. Guglielmi, C.F. Njeh, F. de Terlizzi, D.A. De Serio, A. Scillitani, M. Cammisa, B. Fan, Y. Lu, H.K. Genant, Palangeal quantitative ultrasound, phalangeal morphometric variables, and vertebral fracture discrimination. Calcif. Tissue Int. 72(4), 469–477 (2003). doi:10.1007/s00223-001-1092-0

    Article  CAS  PubMed  Google Scholar 

  147. R. Barkmann, E. Kantorovich, C. Singal, D. Hans, H.K. Genant, M. Heller, C.C. Gluer, A new method for quantitative ultrasound measurements at multiple skeletal sites: first results of precision and fracture discrimination. J. Clin. Densitom. 3(1), 1–7 (2000)

    Article  CAS  PubMed  Google Scholar 

  148. K.T. Khaw, J. Reeve, R. Luben, S. Bingham, A. Welch, N. Wareham, S. Oakes, N. Day, Prediction of total and hip fracture risk in men and women by quantitative ultrasound of the calcaneus: EPIC-Norfolk prospective population study. Lancet 363(9404), 197–202 (2004). doi:10.1016/s0140-6736(03)15325-1

    Article  PubMed  Google Scholar 

  149. T. Yamaguchi, M. Yamamoto, I. Kanazawa, M. Yamauchi, S. Yano, N. Tanaka, E. Nitta, A. Fukuma, S. Uno, T. Sho-no, T. Sugimoto, Quantitative ultrasound and vertebral fractures in patients with type 2 diabetes. J. Bone Miner. Metab. 29(5), 626–632 (2011). doi:10.1007/s00774-011-0265-9

    Article  PubMed  Google Scholar 

  150. S. Patel, S. Hyer, K. Tweed, S. Kerry, K. Allan, A. Rodin, J. Barron, Risk factors for fractures and falls in older women with type 2 diabetes mellitus. Calcif. Tissue. Int. 82(2), 87–91 (2008). doi:10.1007/s00223-007-9082-5

    Article  CAS  PubMed  Google Scholar 

  151. B. Tao, J.M. Liu, H.Y. Zhao, L.H. Sun, W.Q. Wang, X.Y. Li, G. Ning, Differences between measurements of bone mineral densities by quantitative ultrasound and dual-energy X-ray absorptiometry in type 2 diabetic postmenopausal women. J. Clin. Endocrinol. Metab. 93(5), 1670–1675 (2008). doi:10.1210/jc.2007-1760

    Article  CAS  PubMed  Google Scholar 

  152. E.S. Strotmeyer, J.A. Cauley, T.J. Orchard, A.R. Steenkiste, J.S. Dorman, Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes Care 29(2), 306–311 (2006)

    Article  PubMed  Google Scholar 

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  1. Diagnostic and Interventional Radiology, The “Rizzoli” Orthopaedic Institute, Via G. C. Pupilli 1, 40136, Bologna, Italy

    Federico Ponti & Alberto Bazzocchi

  2. Department of Experimental, Diagnostic and Specialty Medicine (DIMES), Division of Radiology S.Orsola-Malpighi Hospital, University of Bologna, Via G. Massarenti 9, 40138, Bologna, Italy

    Federico Ponti, Sara Guerri, Claudia Sassi & Giuseppe Battista

  3. Department of Radiology, University of Foggia, Viale Luigi Pinto 1, 71100, Foggia, Italy

    Giuseppe Guglielmi

  4. Department of Radiology, Scientific Institute “Casa Sollievo della Sofferenza” Hospital, Viale Cappuccini 1, 71013, San Giovanni Rotondo, Foggia, Italy

    Giuseppe Guglielmi

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Ponti, F., Guerri, S., Sassi, C. et al. Imaging of diabetic bone. Endocrine 58, 426–441 (2017). https://doi.org/10.1007/s12020-017-1278-5

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  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-017-1278-5

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