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03-14-2017 | Bone health | Article

Imaging of diabetic bone

Journal: Endocrine

Authors: Federico Ponti, Sara Guerri, Claudia Sassi, Giuseppe Battista, Giuseppe Guglielmi, Alberto Bazzocchi

Publisher: Springer US

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.
Literature
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
7.
A.V. Schwartz, D.E. Sellmeyer, Diabetes, fracture, and bone fragility. Curr. Osteoporos. Rep. 5(3), 105–111 (2007) PubMedCrossRef
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 PubMedCrossRef
9.
M.L. Isidro, B. Ruano, Bone disease in diabetes. Curr. Diabetes Rev. 6(3), 144–155 (2010) PubMedCrossRef
10.
S. Yamagishi, Role of advanced glycation end products (AGEs) in osteoporosis in diabetes. Curr. Drug Targets 12(14), 2096–2102 (2011) PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMed
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 PubMedPubMedCentralCrossRef
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 PubMedPubMedCentralCrossRef
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​ PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 CrossRef
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) PubMedPubMedCentralCrossRef
30.
M.A. Bredella, Perspective: the bone-fat connection. Skeletal Radiol. 39(8), 729–731 (2010). doi: 10.​1007/​s00256-010-0936-y PubMedCrossRef
31.
S. Adami, Bone health in diabetes: considerations for clinical management. Curr. Med. Res. Opin. 25(5), 1057–1072 (2009). doi: 10.​1185/​0300799090280114​7 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
36.
J.J. Minguell, A. Erices, P. Conget, Mesenchymal stem cells. Exp. Biol. Med. (Maywood) 226(6), 507–520 (2001) CrossRef
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) PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentral
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMed
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 PubMedCrossRef
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) PubMed
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
67.
A. Bazzocchi, G. Guglielmi, Vertebral fracture identification. Semin. Musculoskelet. Radiol. 20(4), 317–329 (2016). doi: 10.​1055/​s-0036-1592435 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
70.
W.A. Kalender, Effective dose values in bone mineral measurements by photon absorptiometry and computed tomography. Osteoporos. Int. 2(2), 82–87 (1992) PubMedCrossRef
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 PubMedCrossRef
72.
E. Barnett, B.E. Nordin, The radiological diagnosis of osteoporosis: a new approach. Clin. Radiol. 11, 166–174 (1960) PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
76.
Development Committee of the National Osteoporosis Foundation. Osteoporos. Int. 8(4), S1–S2 (1998). doi: 10.​1007/​pl00020934 CrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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)
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
86.
A. Saller, S. Maggi, G. Romanato, P. Tonin, G. Crepaldi, Diabetes and osteoporosis. Aging Clin. Exp. Res. 20(4), 280–289 (2008) PubMedCrossRef
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) PubMedCrossRef
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) PubMedCrossRef
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
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 CrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
97.
P. Jackuliak, J. Payer, Osteoporosis, fractures, and diabetes. Int. J. Endocrinol. 2014, 820615 (2014). doi: 10.​1155/​2014/​820615 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
105.
C. Cormier, O. L, S. Poriau. TBS in routine clinial practice: proposal. (Medimaps Group, Plan‐les‐Outes, 2012)
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
112.
T.J. Beck, Extending DXA beyond bone mineral density: understanding hip structure analysis. Curr. Osteoporos. Rep. 5(2), 49–55 (2007) PubMedCrossRef
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
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 PubMedPubMedCentralCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMed
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 PubMedPubMedCentralCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 CrossRef
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 CrossRef
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) PubMed
134.
J.B. Vogler 3rd, W.A. Murphy, Bone marrow imaging. Radiology 168(3), 679–693 (1988). doi: 10.​1148/​radiology.​168.​3.​3043546 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedPubMedCentralCrossRef
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 PubMedCrossRef
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) PubMed
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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 PubMedCrossRef
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) PubMedCrossRef

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