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Assessment of bone quality in patients with diabetes mellitus

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Abstract

Substantial evidence exists that diabetes mellitus is associated with an increased risk of osteoporotic fractures. Low bone strength as well as bone extrinsic factors are probably contributing to the increased bone fragility in diabetes. Bone density and quality are important determinants of bone strength. Although bone mineral density (BMD) and the fracture risk assessment tool (FRAX) are very useful clinical tools in assessing bone strength, they may underestimate the fracture risk in diabetes mellitus. Through advances in new technologies such as trabecular bone score (TBS) and peripheral quantitative computed tomography (pQCT), we can better assess the bone quality and fracture risk of patients with diabetes mellitus. Invasive assessments such as microindentation and histomorphometry have been great complement to the existing bone analysis techniques. Bone turnover markers have been found to be altered in diabetes mellitus patients and may be associated with fractures. This review will give a brief summary of the current development and clinical uses of these assessments.

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References

  1. Ogurtsova K, da Rocha Fernandes JD, Huang Y, Linnenkamp U, Guariguata L, Cho NH, Cavan D, Shaw JE, Makaroff LE (2017) IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Res Clin Pract 128:40–50

    Article  PubMed  CAS  Google Scholar 

  2. Siris ES, Adler R, Bilezikian J, Bolognese M, Dawson-Hughes B, Favus MJ, Harris ST, Jan de Beur SM, Khosla S, Lane NE, Lindsay R, Nana AD, Orwoll ES, Saag K, Silverman S, Watts NB (2014) The clinical diagnosis of osteoporosis: a position statement from the National Bone Health Alliance Working Group. Osteoporos Int 25:1439–1443

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  4. Janghorbani M, Van Dam RM, Willett WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505

    Article  PubMed  Google Scholar 

  5. Majumdar SR, Leslie WD, Lix LM, Morin SN, Johansson H, Oden A, McCloskey EV, Kanis JA (2016) Longer duration of diabetes strongly impacts fracture risk assessment: the Manitoba BMD cohort. J Clin Endocrinol Metab 101:4489–4496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Napoli N, Chandran M, Pierroz DD, Abrahamsen B, Schwartz AV, Ferrari SL (2017) Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol 13:208–219

    Article  PubMed  CAS  Google Scholar 

  7. Johnston SS, Conner C, Aagren M, Ruiz K, Bouchard J (2012) Association between hypoglycaemic events and fall-related fractures in Medicare-covered patients with type 2 diabetes. Diabetes Obes Metab 14:634–643

    Article  PubMed  CAS  Google Scholar 

  8. Formiga F, Chivite D, Ruiz D, Navarro M, Perez Castejon JM, Duaso E, Montero A, Lopez-Soto A, Corbella X (2015) Clinical evidence of diabetes mellitus end-organ damage as risk factor for falls complicated by hip fracture: a multi-center study of 1225 patients. Diabetes Res Clin Pract 109:233–237

    Article  PubMed  Google Scholar 

  9. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38

    Article  PubMed  CAS  Google Scholar 

  10. Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, Johnson KC, Margolis KL (2006) Risk of fracture in women with type 2 diabetes: the Women's Health Initiative observational study. J Clin Endocrinol Metab 91:3404–3410

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  12. Maggio AB, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. J Pediatr Endocrinol Metab 23:697–707

    Article  PubMed  CAS  Google Scholar 

  13. Hadjidakis DJ, Raptis AE, Sfakianakis M, Mylonakis A, Raptis SA (2006) Bone mineral density of both genders in type 1 diabetes according to bone composition. J Diabetes Complicat 20:302–307

    Article  PubMed  Google Scholar 

  14. Miazgowski T, Czekalski S (1998) A 2-year follow-up study on bone mineral density and markers of bone turnover in patients with long-standing insulin-dependent diabetes mellitus. Osteoporos Int 8:399–403

    Article  PubMed  CAS  Google Scholar 

  15. Neumann T, Samann A, Lodes S, Kastner B, Franke S, Kiehntopf M, Hemmelmann C, Lehmann T, Muller UA, Hein G et al (2011) Glycaemic control is positively associated with prevalent fractures but not with bone mineral density in patients with type 1 diabetes. Diabet Med 28:872–875

    Article  PubMed  CAS  Google Scholar 

  16. Mastrandrea LD, Wactawski-Wende J, Donahue RP, Hovey KM, Clark A, Quattrin T (2008) Young women with type 1 diabetes have lower bone mineral density that persists over time. Diabetes Care 31:1729–1735

    Article  PubMed  PubMed Central  Google Scholar 

  17. AboElAsrar MA, Elbarbary NS, Elshennawy DE, Omar AM (2012) Insulin-like growth factor-1 cytokines cross-talk in type 1 diabetes mellitus: relationship to microvascular complications and bone mineral density. Cytokine 59:86–93

    Article  PubMed  CAS  Google Scholar 

  18. Slade JM, Coe LM, Meyer RA, McCabe LR (2012) Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes. J Diabetes Complicat 26:1–9

    Article  PubMed  Google Scholar 

  19. Gogas Yavuz D, Keskin L, Kiyici S, Sert M, Yazici D, Sahin I, Yuksel M, Deyneli O, Aydin H, Tuncel E et al (2011) Vitamin D receptor gene BsmI, FokI, ApaI, TaqI polymorphisms and bone mineral density in a group of Turkish type 1 diabetic patients. Acta Diabetol 48:329–336

    Article  PubMed  CAS  Google Scholar 

  20. Abd El Dayem SM, El-Shehaby AM, Abd El Gafar A, Fawzy A, Salama H (2011) Bone density, body composition, and markers of bone remodeling in type 1 diabetic patients. Scand J Clin Lab Invest 71:387–393

    Article  PubMed  CAS  Google Scholar 

  21. Heilman K, Zilmer M, Zilmer K, Tillmann V (2009) Lower bone mineral density in children with type 1 diabetes is associated with poor glycemic control and higher serum ICAM-1 and urinary isoprostane levels. J Bone Miner Metab 27:598–604

    Article  PubMed  CAS  Google Scholar 

  22. Hamilton EJ, Rakic V, Davis WA, Chubb SA, Kamber N, Prince RL, Davis TM (2009) Prevalence and predictors of osteopenia and osteoporosis in adults with type 1 diabetes. Diabet Med 26:45–52

    Article  PubMed  CAS  Google Scholar 

  23. Danielson KK, Elliott ME, LeCaire T, Binkley N, Palta M (2009) Poor glycemic control is associated with low BMD detected in premenopausal women with type 1 diabetes. Osteoporos Int 20:923–933

    Article  PubMed  CAS  Google Scholar 

  24. Miazgowski T, Pynka S, Noworyta-Zietara M, Krzyzanowska-Swiniarska B, Pikul R (2007) Bone mineral density and hip structural analysis in type 1 diabetic men. Eur J Endocrinol 156:123–127

    Article  PubMed  CAS  Google Scholar 

  25. Karaguzel G, Akcurin S, Ozdem S, Boz A, Bircan I (2006) Bone mineral density and alterations of bone metabolism in children and adolescents with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 19:805–814

    PubMed  Google Scholar 

  26. Strotmeyer ES, Cauley JA, Orchard TJ, Steenkiste AR, Dorman JS (2006) Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes Care 29:306–311

    Article  PubMed  Google Scholar 

  27. Salvatoni A, Mancassola G, Biasoli R, Cardani R, Salvatore S, Broggini M, Nespoli L (2004) Bone mineral density in diabetic children and adolescents: a follow-up study. Bone 34:900–904

    Article  PubMed  Google Scholar 

  28. Ingberg CM, Palmer M, Aman J, Arvidsson B, Schvarcz E, Berne C (2004) Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255:392–398

    Article  PubMed  Google Scholar 

  29. Heap J, Murray MA, Miller SC, Jalili T, Moyer-Mileur LJ (2004) Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr 144:56–62

    Article  PubMed  CAS  Google Scholar 

  30. Liu EY, Wactawski-Wende J, Donahue RP, Dmochowski J, Hovey KM, Quattrin T (2003) Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care 26:2365–2369

    Article  PubMed  Google Scholar 

  31. Rachon D, Mysliwska J, Suchecka-Rachon K, Semetkowska-Jurkiewicz B, Zorena K, Lysiak-Szydlowska W (2003) Serum interleukin-6 levels and bone mineral density at the femoral neck in post-menopausal women with type 1 diabetes. Diabet Med 20:475–480

    Article  PubMed  CAS  Google Scholar 

  32. Gunczler P, Lanes R, Paoli M, Martinis R, Villaroel O, Weisinger JR (2001) Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14:525–528

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  34. Hampson G, Evans C, Petitt RJ, Evans WD, Woodhead SJ, Peters JR, Ralston SH (1998) Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia 41:1314–1320

    Article  PubMed  CAS  Google Scholar 

  35. Lunt H, Florkowski CM, Cundy T, Kendall D, Brown LJ, Elliot JR, Wells JE, Turner JG (1998) A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes Res Clin Pract 40:31–38

    Article  PubMed  CAS  Google Scholar 

  36. Olmos JM, Perez-Castrillon JL, Garcia MT, Garrido JC, Amado JA, Gonzalez-Macias J (1994) Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner 26:1–8

    Article  PubMed  CAS  Google Scholar 

  37. Pan H, Wu N, Yang T, He W (2014) Association between bone mineral density and type 1 diabetes mellitus: a meta-analysis of cross-sectional studies. Diabetes Metab Res Rev 30:531–542

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  39. Kao WH, Kammerer CM, Schneider JL, Bauer RL, Mitchell BD (2003) Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res 34:399–406

    Article  PubMed  Google Scholar 

  40. Majima T, Komatsu Y, Yamada T, Koike Y, Shigemoto M, Takagi C, Hatanaka I, Nakao K (2005) Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 16:907–913

    Article  PubMed  CAS  Google Scholar 

  41. Barrett-Connor E, Holbrook TL (1992) Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337

    Article  PubMed  CAS  Google Scholar 

  42. Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512

    Article  PubMed  CAS  Google Scholar 

  43. de Liefde II, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam study. Osteoporos Int 16:1713–1720

    Article  PubMed  Google Scholar 

  44. Sosa M, Dominguez M, Navarro MC, Segarra MC, Hernandez D, de Pablos P, Betancor P (1996) Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complicat 10:201–205

    Article  PubMed  CAS  Google Scholar 

  45. Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, Cooper C (2004) Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire cohort study: evidence for an indirect effect of insulin resistance? Diabetologia 47:1963–1968

    Article  PubMed  CAS  Google Scholar 

  46. Bridges MJ, Moochhala SH, Barbour J, Kelly CA (2005) Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol 42:82–86

    Article  PubMed  CAS  Google Scholar 

  47. Schwartz AV, Sellmeyer DE, Strotmeyer ES, Tylavsky FA, Feingold KR, Resnick HE, Shorr RI, Nevitt MC, Black DM, Cauley JA et al (2005) Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596–603

    Article  PubMed  Google Scholar 

  48. Rakic V, Davis WA, Chubb SA, Islam FM, Prince RL, Davis TM (2006) Bone mineral density and its determinants in diabetes: the Fremantle diabetes study. Diabetologia 49:863–871

    Article  PubMed  CAS  Google Scholar 

  49. Hadzibegovic I, Miskic B, Cosic V, Prvulovic D, Bistrovic D (2008) Increased bone mineral density in postmenopausal women with type 2 diabetes mellitus. Ann Saudi Med 28:102–104

    Article  PubMed  Google Scholar 

  50. Anaforoglu I, Nar-Demirer A, Bascil-Tutuncu N, Ertorer ME (2009) Prevalence of osteoporosis and factors affecting bone mineral density among postmenopausal Turkish women with type 2 diabetes. J Diabetes Complicat 23:12–17

    Article  PubMed  Google Scholar 

  51. Ma L, Oei L, Jiang L, Estrada K, Chen H, Wang Z, Yu Q, Zillikens MC, Gao X, Rivadeneira F (2012) Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 27:319–332

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, Donaldson MG, Cauley JA, Harris TB, Koster A, Womack CR, Palermo L, Black DM, Study of Osteoporotic Fractures (SOF) Research Group, Osteoporotic Fractures in Men (MrOS) Research Group, Health, Aging, and Body Composition (Health ABC) Research Group (2011) Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305:2184–2192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  54. Martineau P, Leslie WD, Johansson H, Oden A, McCloskey EV, Hans D, Kanis JA (2017) Clinical utility of using lumbar spine trabecular bone score to adjust fracture probability: the Manitoba BMD cohort. J Bone Miner Res 32:1568–1574

    Article  PubMed  Google Scholar 

  55. 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  PubMed  CAS  Google Scholar 

  56. 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  PubMed  CAS  Google Scholar 

  57. 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  PubMed  CAS  Google Scholar 

  58. Shah V, Pyle L, Joshee P, Ostendorf D, Kohrt WM, Alman A, Snell-Bergeon JK (2017) Trabecular bone score is lower in adults with type 1 diabetes and is related to visceral and pericardial fat but not body mass index or subcutaneous fat. Endocr Rev 38:S1 

  59. Syversen U, Reseland J, Eriksen EF, Mynarek IM, Iversen TSJ, Basso T, Aasarød KM, Åsvold BO, Mosti MP, Stunes AK (2017) Impaired bone quality, assessed by trabecular bone score and in vivo micro indentation, in men with type 1 diabetes mellitus. Calcif Tissue Int 100:S29

    Article  CAS  Google Scholar 

  60. Shah VN, Sippl R, Joshee P, Pyle L, Kohrt WM, Schauer IE, Snell-Bergeon JK (2018) Trabecular bone quality is lower in adults with type 1 diabetes and is negatively associated with insulin resistance. Osteoporos Int 29:733–739

    Article  PubMed  CAS  Google Scholar 

  61. Gilmour J, Colquhoun A, Wu W, Kim S (2018) Type 1 diabetes and bone microarchitecture assessment with trabecular bone score (TBS): a descriptive study. J Clin Densitom 21:27

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  63. 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 

  64. Zhukouskaya VV, Eller-Vainicher C, Gaudio A, Privitera F, Cairoli E, Ulivieri FM, Palmieri S, Morelli V, Grancini V, Orsi E et al (2016) The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients. Osteoporos Int 27:49–56

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  67. De Araújo I, Salmon C, Nogueira-Barbosa M, Luchini S, De Paula F (2017) Marrow adipose tissue, trabecular bone score and osteocalcin as parameters of bone quality in type 2 diabetes mellitus. J Bone Miner Res 32:S316

    Google Scholar 

  68. Buni M, Ambrose CG, McCormick J, Fisher-Hoch S, Rianon N (2017) The utility of trabecular bone score in evaluating bone quality in Hispanic population with type 2 diabetes. J Bone Miner Res 32:S245

    Google Scholar 

  69. Payer J, Jackuliak P, Kuzma M, Killinger Z (2017) Metabolic compensation of type 2 diabetes and bone quality. Endocr Rev 38:S1 

  70. Torres MM, Perez MDA, Martin AG, Rodriguez CN, Córdova RM, Serrano RN (2017) Trabecular bone score in type 2 diabetes mellitus: preliminary data of cross-sectional case-control study. J Bone Miner Res 31:S1 

  71. Xue Y, Baker AL, Nader S, Orlander P, Sanchez AJ, Kellam J, Rianon NJ, Ambrose CG (2017) Lumbar spine trabecular bone score (TBS) reflects diminished bone quality in patients with diabetes mellitus and oral glucocorticoid therapy. J Clin Densitom 21:185–192

  72. Jain RK, Zeytinoglu M, Vokes TJ (2017) Diabetes mellitus and trabecular bone score (TBS) in caucasians and African Americans referred for bone densitometry. Endocr Rev 38:S1

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  75. Hans D, Stenova E, Lamy O (2017) The trabecular bone score (TBS) complements DXA and the FRAX as a fracture risk assessment tool in routine clinical practice. Curr Osteoporos Rep 15:521–531

    Article  PubMed  Google Scholar 

  76. Pawlowska M, Bilezikian JP (2016) Beyond DXA: advances in clinical applications of new bone imaging TECHNOLOGY. Endocr Pract 22:990–998

    Article  PubMed  PubMed Central  Google Scholar 

  77. Macneil JA, Boyd SK (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213

    Article  PubMed  Google Scholar 

  78. Ishikawa K, Fukui T, Nagai T, Kuroda T, Hara N, Yamamoto T, Inagaki K, Hirano T (2015) Type 1 diabetes patients have lower strength in femoral bone determined by quantitative computed tomography: a cross-sectional study. J Diab Investig 6:726–733

    Article  CAS  Google Scholar 

  79. Saha MT, Sievanen H, Salo MK, Tulokas S, Saha HH (2009) Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int 20:1401–1406

    Article  PubMed  CAS  Google Scholar 

  80. Shanbhogue VV, Hansen S, Frost M, Jorgensen NR, Hermann AP, Henriksen JE, Brixen K (2015) 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 30:2188–2199

    Article  PubMed  CAS  Google Scholar 

  81. Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu CT, Boyd SK, McLean RR, Broe KE, Kiel DP et al (2017) Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT study. J Bone Miner Res 33:54–62

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

    Article  PubMed  Google Scholar 

  83. Roe TF, Mora S, Costin G, Kaufman F, Carlson ME, Gilsanz V (1991) Vertebral bone density in insulin-dependent diabetic children. Metabolism 40:967–971

    Article  PubMed  CAS  Google Scholar 

  84. Lettgen B, Hauffa B, Mohlmann C, Jeken C, Reiners C (1995) Bone mineral density in children and adolescents with juvenile diabetes: selective measurement of bone mineral density of trabecular and cortical bone using peripheral quantitative computed tomography. Horm Res 43:173–175

    Article  PubMed  CAS  Google Scholar 

  85. Moyer-Mileur LJ, Dixon SB, Quick JL, Askew EW, Murray MA (2004) Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr 145:662–669

    Article  PubMed  Google Scholar 

  86. Bechtold S, Putzker S, Bonfig W, Fuchs O, Dirlenbach I, Schwarz HP (2007) Bone size normalizes with age in children and adolescents with type 1 diabetes. Diabetes Care 30:2046–2050

    Article  PubMed  Google Scholar 

  87. Roggen I, Gies I, Vanbesien J, Louis O, De Schepper J (2013) Trabecular bone mineral density and bone geometry of the distal radius at completion of pubertal growth in childhood type 1 diabetes. Horm Res Paediatr 79:68–74

    Article  PubMed  CAS  Google Scholar 

  88. Starup-Linde J, Lykkeboe S, Gregersen S, Hauge EM, Langdahl BL, Handberg A, Vestergaard P (2016) Bone structure and predictors of fracture in type 1 and type 2 diabetes. J Clin Endocrinol Metab 101:928–936

    Article  PubMed  CAS  Google Scholar 

  89. Kuroda T, Ishikawa K, Nagai T, Fukui T, Hirano T, Inagaki K (2017) Quadrant analysis of quantitative computed tomography scans of the femoral neck reveals superior region-specific weakness in young and middle-aged men with type 1 diabetes mellitus. J Clin Densitom 21:172–178

  90. Verroken C, Pieters W, Beddeleem L, Goemaere S, Zmierczak HG, Shadid S, Kaufman JM, Lapauw B (2017) Cortical bone size deficit in adult patients with type 1 diabetes mellitus. J Clin Endocrinol Metab 102:2887–2895

    Article  PubMed  Google Scholar 

  91. Maratova K, Soucek O, Matyskova J, Hlavka Z, Petruzelkova L, Obermannova B, Pruhova S, Kolouskova S, Sumnik Z (2018) Muscle functions and bone strength are impaired in adolescents with type 1 diabetes. Bone 106:22–27

    Article  PubMed  Google Scholar 

  92. Register TC, Lenchik L, Hsu FC, Lohman KK, Freedman BI, Bowden DW, Carr JJ (2006) Type 2 diabetes is not independently associated with spinal trabecular volumetric bone mineral density measured by QCT in the diabetes heart study. Bone 39:628–633

    Article  PubMed  CAS  Google Scholar 

  93. Melton LJ 3rd, Riggs BL, Leibson CL, Achenbach SJ, Camp JJ, Bouxsein ML, Atkinson EJ, Robb RA, Khosla S (2008) A bone structural basis for fracture risk in diabetes. J Clin Endocrinol Metab 93:4804–4809

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE (2010) Bone mass and strength in older men with type 2 diabetes: the osteoporotic fractures in men study. J Bone Miner Res 25:285–291

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  96. Shu A, Yin MT, Stein E, Cremers S, Dworakowski E, Ives R, Rubin MR (2012) Bone structure and turnover in type 2 diabetes mellitus. Osteoporos Int 23:635–641

    Article  PubMed  CAS  Google Scholar 

  97. Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res 28:313–324

    Article  PubMed  PubMed Central  Google Scholar 

  98. Kiyohara N, Yamamoto M, Sugimoto T (2015) Discordance between prevalent vertebral fracture and vertebral strength estimated by the finite element method based on quantitative computed tomography in patients with type 2 diabetes mellitus. PLoS One 10:e0144496

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Yu EW, Putman MS, Derrico N, Abrishamanian-Garcia G, Finkelstein JS, Bouxsein ML (2015) Defects in cortical microarchitecture among African-American women with type 2 diabetes. Osteoporos Int 26:673–679

    Article  PubMed  CAS  Google Scholar 

  100. Heilmeier U, Carpenter DR, Patsch JM, Harnish R, Joseph GB, Burghardt AJ, Baum T, Schwartz AV, Lang TF, Link TM (2015) Volumetric femoral BMD, bone geometry, and serum sclerostin levels differ between type 2 diabetic postmenopausal women with and without fragility fractures. Osteoporos Int 26:1283–1293

    Article  PubMed  CAS  Google Scholar 

  101. Shanbhogue VV, Hansen S, Frost M, Jorgensen NR, Hermann AP, Henriksen JE, Brixen K (2016) Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur J Endocrinol 174:115–124

    Article  PubMed  CAS  Google Scholar 

  102. Patsch JM, Rasul S, Huber FA, Leitner K, Thomas A, Kocijan R, Boutroy S, Weber M, Resch H, Kainberger F, Schüller-Weidekamm C, Kautzky-Willer A (2017) Similarities in trabecular hypertrophy with site-specific differences in cortical morphology between men and women with type 2 diabetes mellitus. PLoS One 12:e0174664

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  103. Paccou J, Ward KA, Jameson KA, Dennison EM, Cooper C, Edwards MH (2016) Bone microarchitecture in men and women with diabetes: the importance of cortical porosity. Calcif Tissue Int 98:465–473

    Article  PubMed  CAS  Google Scholar 

  104. Allen MR, McNerny EM, Organ JM, Wallace JM (2015) True gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo. J Bone Miner Res 30:1539–1550

    Article  PubMed  PubMed Central  Google Scholar 

  105. Malgo F, Hamdy NA, Papapoulos SE, Appelman-Dijkstra NM (2015) Bone material strength as measured by microindentation in vivo is decreased in patients with fragility fractures independently of bone mineral density. J Clin Endocrinol Metab 100:2039–2045

    Article  PubMed  CAS  Google Scholar 

  106. Furst JR, Bandeira LC, Fan WW, Agarwal S, Nishiyama KK, McMahon DJ, Dworakowski E, Jiang H, Silverberg SJ, Rubin MR (2016) Advanced glycation Endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab 101:2502–2510

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Armas LA, Akhter MP, Drincic A, Recker RR (2012) Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone 50:91–96

    Article  PubMed  Google Scholar 

  108. Hamann C, Goettsch C, Mettelsiefen J, Henkenjohann V, Rauner M, Hempel U, Bernhardt R, Fratzl-Zelman N, Roschger P, Rammelt S, Günther KP, Hofbauer LC (2011) Delayed bone regeneration and low bone mass in a rat model of insulin-resistant type 2 diabetes mellitus is due to impaired osteoblast function. Am J Physiol Endocrinol Metab 301:E1220–E1228

    Article  PubMed  CAS  Google Scholar 

  109. Abbassy MA, Watari I, Soma K (2010) The effect of diabetes mellitus on rat mandibular bone formation and microarchitecture. Eur J Oral Sci 118:364–369

    Article  PubMed  Google Scholar 

  110. Picke AK, Gordaliza Alaguero I, Campbell GM, Gluer CC, Salbach-Hirsch J, Rauner M, Hofbauer LC, Hofbauer C (2016) Bone defect regeneration and cortical bone parameters of type 2 diabetic rats are improved by insulin therapy. Bone 82:108–115

    Article  PubMed  CAS  Google Scholar 

  111. Follak N, Kloting I, Wolf E, Merk H (2004) Improving metabolic control reverses the histomorphometric and biomechanical abnormalities of an experimentally induced bone defect in spontaneously diabetic rats. Calcif Tissue Int 74:551–560

    Article  PubMed  CAS  Google Scholar 

  112. Klein, Frost HM, Sedlin E (1964) A pilot study of lamellar bone physiology in diabetes mellitus. Henry Ford Hosp Med Bull 12:55–62

    PubMed  CAS  Google Scholar 

  113. Leite Duarte ME, da Silva RD (1996) Histomorphometric analysis of the bone tissue in patients with non-insulin-dependent diabetes (DMNID). Rev Hosp Clin 51:7–11

    CAS  Google Scholar 

  114. Starup-Linde J, Eriksen SA, Lykkeboe S, Handberg A, Vestergaard P (2014) Biochemical markers of bone turnover in diabetes patients--a meta-analysis, and a methodological study on the effects of glucose on bone markers. Osteoporos Int 25:1697–1708

    Article  PubMed  CAS  Google Scholar 

  115. Pater A, Sypniewska G, Pilecki O (2010) Biochemical markers of bone cell activity in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 23:81–86

    Article  PubMed  CAS  Google Scholar 

  116. Alexopoulou O, Jamart J, Devogelaer JP, Brichard S, de Nayer P, Buysschaert M (2006) Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabete Metab 32:453–458

    Article  PubMed  CAS  Google Scholar 

  117. Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363

    Article  PubMed  CAS  Google Scholar 

  118. Ardawi MS, Akhbar DH, Alshaikh A, Ahmed MM, Qari MH, Rouzi AA, Ali AY, Abdulrafee AA, Saeda MY (2013) Increased serum sclerostin and decreased serum IGF-1 are associated with vertebral fractures among postmenopausal women with type-2 diabetes. Bone 56:355–362

    Article  PubMed  CAS  Google Scholar 

  119. Yamamoto M, Yamaguchi T, Nawata K, Yamauchi M, Sugimoto T (2012) Decreased PTH levels accompanied by low bone formation are associated with vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 97:1277–1284

    Article  PubMed  CAS  Google Scholar 

  120. Rubin MR, Patsch JM (2016) Assessment of bone turnover and bone quality in type 2 diabetic bone disease: current concepts and future directions. Bone Res 4:16001

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  121. Jiajue R, Jiang Y, Wang O, Li M, Xing X, Cui L, Yin J, Xu L, Xia W (2014) Suppressed bone turnover was associated with increased osteoporotic fracture risks in non-obese postmenopausal Chinese women with type 2 diabetes mellitus. Osteoporosis Int 25:1999–2005

    Article  CAS  Google Scholar 

  122. Sarkar PD, Choudhury AB (2013) Relationships between serum osteocalcin levels versus blood glucose, insulin resistance and markers of systemic inflammation in central Indian type 2 diabetic patients. Eur Rev Med Pharmacol Sci 17:1631–1635

    PubMed  CAS  Google Scholar 

  123. Movahed A, Larijani B, Nabipour I, Kalantarhormozi M, Asadipooya K, Vahdat K, Akbarzadeh S, Farrokhnia M, Assadi M, Amirinejad R, Bargahi A, Sanjdideh Z (2012) Reduced serum osteocalcin concentrations are associated with type 2 diabetes mellitus and the metabolic syndrome components in postmenopausal women: the crosstalk between bone and energy metabolism. J Bone Miner Metab 30:683–691

    Article  PubMed  CAS  Google Scholar 

  124. Kanazawa I, Yamaguchi T, Sugimoto T (2011) Serum insulin-like growth factor-I is a marker for assessing the severity of vertebral fractures in postmenopausal women with type 2 diabetes mellitus. Osteoporos Int 22:1191–1198

    Article  PubMed  CAS  Google Scholar 

  125. Kanazawa I, Yamaguchi T, Yamamoto M, Sugimoto T (2010) Relationship between treatments with insulin and oral hypoglycemic agents versus the presence of vertebral fractures in type 2 diabetes mellitus. J Bone Miner Metab 28:554–560

    Article  PubMed  CAS  Google Scholar 

  126. Hein GE (2006) Glycation endproducts in osteoporosis--is there a pathophysiologic importance? Clin Chim Acta 371:32–36

    Article  PubMed  CAS  Google Scholar 

  127. Gilbert L, He X, Farmer P, Boden S, Kozlowski M, Rubin J, Nanes MS (2000) Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 141:3956–3964

    Article  PubMed  CAS  Google Scholar 

  128. Glantschnig H, Fisher JE, Wesolowski G, Rodan GA, Reszka AA (2003) M-CSF, TNFalpha and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ 10:1165–1177

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  130. Saito M, Fujii K, Marumo K (2006) Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tissue Int 79:160–168

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  132. DeShields SC, Cunningham TD (2018) Comparison of osteoporosis in US adults with type 1 and type 2 diabetes mellitus. J Endocrinol Investig. https://doi.org/10.1007/s40618-018-0828-x

  133. Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporos Int 18:427–444

    Article  PubMed  CAS  Google Scholar 

  134. Thrailkill KM, Lumpkin CK, Bunn RC, Kemp SF, Fowlkes JL (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Phys Endocrinol Metab 289:E735–E745

    Article  CAS  Google Scholar 

  135. Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22:1317–1328

    Article  PubMed  CAS  Google Scholar 

  136. Compston JE, Flahive J, Hosmer DW, Watts NB, Siris ES, Silverman S, Saag KG, Roux C, Rossini M, Pfeilschifter J, Nieves JW, Netelenbos JC, March L, LaCroix AZ, Hooven FH, Greenspan SL, Gehlbach SH, Díez-Pérez A, Cooper C, Chapurlat RD, Boonen S, Anderson FA Jr, Adami S, Adachi JD, for the GLOW Investigators (2014) Relationship of weight, height, and body mass index with fracture risk at different sites in postmenopausal women: the global longitudinal study of osteoporosis in women (GLOW). J Bone Miner Res 29:487–493

    Article  PubMed  PubMed Central  Google Scholar 

  137. Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 26:496–502

    Article  PubMed  Google Scholar 

  138. Chan MY, Frost SA, Center JR, Eisman JA, Nguyen TV (2014) Relationship between body mass index and fracture risk is mediated by bone mineral density. J Bone Miner Res 29:2327–2335

    Article  PubMed  Google Scholar 

  139. Starup-Linde J, Lykkeboe S, Gregersen S, Hauge EM, Langdahl BL, Handberg A, Vestergaard P (2016) Differences in biochemical bone markers by diabetes type and the impact of glucose. Bone 83:149–155

    Article  PubMed  CAS  Google Scholar 

  140. Gandhi A, Beam HA, O'Connor JP, Parsons JR, Lin SS (2005) The effects of local insulin delivery on diabetic fracture healing. Bone 37:482–490

    Article  PubMed  CAS  Google Scholar 

  141. Fulzele K, DiGirolamo DJ, Liu Z, Xu J, Messina JL, Clemens TL (2007) Disruption of the insulin-like growth factor type 1 receptor in osteoblasts enhances insulin signaling and action. J Biol Chem 282:25649–25658

    Article  PubMed  CAS  Google Scholar 

  142. Miyake H, Kanazawa I, Sugimoto T (2017) Decreased Serum Insulin-like Growth Factor-I is a Risk Factor for Non-vertebral Fractures in Diabetic Postmenopausal Women. Intern Med 56:269–273

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  143. Abrahamsen B, Rohold A, Henriksen JE, Beck-Nielsen H (2000) Correlations between insulin sensitivity and bone mineral density in non-diabetic men. Diabet Med 17:124–129

    Article  PubMed  CAS  Google Scholar 

  144. Shanbhogue VV, Finkelstein JS, Bouxsein ML, Yu EW (2016) Association between insulin resistance and bone structure in nondiabetic postmenopausal women. J Clin Endocrinol Metab 101:3114–3122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  145. Hernandez JL, Olmos JM, Pariente E, Martinez J, Valero C, Garcia-Velasco P, Nan D, Llorca J, Gonzalez-Macias J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17:955–961

    Article  PubMed  Google Scholar 

  146. Verroken C, Zmierczak HG, Goemaere S, Kaufman JM, Lapauw B (2017) Insulin resistance is associated with smaller cortical bone size in nondiabetic men at the age of peak bone mass. J Clin Endocrinol Metab 102:1807–1815

    Article  PubMed  Google Scholar 

  147. von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the rancho Bernardo study. Osteoporos Int 18:1337–1344

    Article  Google Scholar 

  148. Tonks KT, White CP, Center JR, Samocha-Bonet D, Greenfield JR (2017) Bone turnover is suppressed in insulin resistance, independent of adiposity. J Clin Endocrinol Metab 102:1112–1121

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by a grant from The Ministry of Science and Technology of the Peoples Republic of China (National Science and Technology Major Projects for Major New Drugs Innovation and Development 2008ZX09312-016), National Natural Science Foundation of China (No. 81070687,81170805 and 81670714), Beijing Natural Science Foundation (No. 7121012) and Scientific Research Foundation of Beijing Medical Development (No. 2007-3029), National Key Program of Clinical Science (WBYZ2011-873), CAMS Innovation Fund for Medical Sciences (No. 2016-I2M-3-003).

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  1. Department of Endocrinology, Key Laboratory of Endocrinology, Ministry of Health, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Shuaifuyuan No. 1, Wangfujing, Dongcheng District, Beijing, 100730, China

    N. Jiang & W. Xia

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Jiang, N., Xia, W. Assessment of bone quality in patients with diabetes mellitus. Osteoporos Int 29, 1721–1736 (2018). https://doi.org/10.1007/s00198-018-4532-7

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