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Published in:

01-03-2013 | Original Paper

Clinical Aspects of Diabetic Bone Disease: An Update

Author: Ann V. Schwartz

Published in: Clinical & Translational Metabolism | Issue 1/2013

Abstract

Older adults with type 2 diabetes have a higher risk of fracture but do not have decrements in bone density. The reasons for greater bone fragility in diabetes are still not clearly understood, but progress has been made in identifying potential contributors. With new imaging techniques, increased cortical porosity has been identified as a possible contributing factor to bone fragility. Cortical porosity may be especially detrimental to bone strength in the presence of higher levels of advanced glycation end products. Initial results have reported higher levels of marrow adiposity in diabetic men, suggesting that diabetes may contribute to marrow stem-cell lineage allocation toward adipocytes rather than osteoblasts. Higher levels of sclerostin have also been observed in diabetic patients, indicating that osteocyte function may play a role in diabetic bone. An important clinical question, “How to best predict fracture in diabetic patients?” has been addressed with studies demonstrating that BMD T-score and FRAX score predict fractures but underestimate absolute risk in diabetic patients. For prevention of fractures, there is now evidence from a clinical trial that intensive glycemic control does not increase fracture or fall risk but also does not reduce these outcomes. The pursuit of these new findings promises to provide insights into the reasons for greater fragility of diabetic bone and the best methods for fracture prevention in this population.

Miao J, Brismar K, Nyren O, Ugarph-Morawski A, Ye W. Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care. 2005;28:2850–5.CrossRefPubMed

Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24:1192–7.CrossRefPubMed

Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86:32–8.CrossRefPubMed

Ottenbacher KJ, Ostir GV, Peek MK, Goodwin JS, Markides KS. Diabetes mellitus as a risk factor for hip fracture in Mexican–American older adults. J Gerontol A Biol Sci Med Sci. 2002;57:M648–53.CrossRefPubMed

Holmberg AH, Johnell O, Nilsson PM, Nilsson JA, Berglund G, Akesson K. Risk factors for hip fractures in a middle-aged population: a study of 33,000 men and women. Osteoporos Int. 2005;16:2185–94.CrossRefPubMed

Vestergaard P, Rejnmark L, Mosekilde L. Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia. 2005;48:1292–9.CrossRefPubMed

Ahmed LA, Joakimsen RM, Berntsen GK, Fønnebø V, Schirmer H. Diabetes mellitus and the risk of non-vertebral fractures: the Tromsø study. Osteoporos Int. 2006;17:495–500.CrossRefPubMed

Janghorbani M, Feskanich D, Willett WC, Hu F. Prospective study of diabetes and risk of hip fracture: the Nurses’ Health Study. Diabetes Care. 2006;29:1573–8.CrossRefPubMed

Melton LJ III, Leibson CL, Achenbach SJ, Therneau TM, Khosla S. Fracture risk in type 2 diabetes: update of a population-based study. J Bone Miner Res. 2008;23:1334–42.CrossRefPubMed

10.

Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes-a meta-analysis. Osteoporos Int. 2007;18:427–44.CrossRefPubMed

11.

Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, et al. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165:1612–7.CrossRefPubMed

12.

Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, et al. Risk of fracture among women with type 2 diabetes: the women’s health initiative observational study. J Clin Endocrinol Metab. 2006;91:3404–10.CrossRefPubMed

13.

de Liefde I, van der Klift M, de Laet CE, van Daele PL, Hofman A, Pols HA. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int. 2005;16:1713–20.CrossRefPubMed

14.

Forsen L, Meyer HE, Midthjell K, Edna TH. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia. 1999;42:920–5.CrossRefPubMed

15.

Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res. 2007;22:1317–28.CrossRefPubMed

16.

Schwartz AV. Impact of diabetes and its treatment on bone. Clinic Rev Bone Miner Metab. 2009;7:249–60.CrossRef

17.

Schwartz AV, Hillier TA, Sellmeyer DE, Resnick HE, Gregg E, Ensrud KE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care. 2002;25:1749–54.CrossRefPubMed

18.

Maurer MS, Burcham J, Cheng H. Diabetes mellitus is associated with an increased risk of falls in elderly residents of a long-term care facility. J Gerontol A Biol Sci Med Sci. 2005;60:1157–62.CrossRefPubMed

19.

Keegan TH, Schwartz AV, Bauer DC, Sellmeyer DE, Kelsey JL. Effect of alendronate on bone mineral density and biochemical markers of bone turnover in type 2 diabetic women: the fracture intervention trial. Diabetes Care. 2004;27:1547–53.CrossRefPubMed

20.

Schwartz AV, Sellmeyer DE, Strotmeyer ES, Tylavsky FA, Feingold KR, Resnick HE, et al. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res. 2005;20:596–603.CrossRefPubMed

21.

Cauley JA, Lui LY, Barnes D, Ensrud KE, Zmuda JM, Hillier TA, et al. Successful skeletal aging: a marker of low fracture risk and longevity. The Study of Osteoporotic Fractures (SOF). J Bone Miner Res. 2009;24:134–43.CrossRefPubMed

22.

Strotmeyer ES, Boudreau RM, Marshall LM, Schwartz AV, Bauer DC, Barrett-Connor E, et al. Higher bone mineral denisty loss in older men with diabetes: The Osteoporotic Fractures in Men Study. In ASBMR 30th annual meeting, 2008. Montreal, ASBMR; 2008.

23.

Hillier TA, Stone KL, Bauer DC, Rizzo JH, Pedula KL, Cauley JA, et al. Evaluating the value of repeat bone mineral density measurement and prediction of fractures in older women: the study of osteoporotic fractures. Arch Intern Med. 2007;167:155–60.CrossRefPubMed

24.

Loke YK, Singh S, Furberg CD. Long-term use of thiazolidinediones and fractures in type 2 diabetes: a meta-analysis. CMAJ. 2009;180:32–9.CrossRefPubMed

25.

Melton LJ 3rd, Riggs BL, Leibson CL, Achenbach SJ, Camp JJ, Bouxsein ML, et al. A bone structural basis for fracture risk in diabetes. J Clin Endocrinol Metab. 2008;93:4804–9.CrossRefPubMed

26.

Petit M, Paudel ML, Taylor B, Hughes J, Strotmeyer ES, Schwartz AV, et al. Bone mass and strength in older men with type 2 diabetes: the Osteoporotic Fractures in Men Study. J Bone Miner Res. 2010;25:285–91.CrossRefPubMed

27.

Seeman E. Periosteal bone formation–a neglected determinant of bone strength. N Engl J Med. 2003;349:320–3.CrossRefPubMed

28.

Yang L, Peel N, Clowes JA, McCloskey EV, Eastell R. Use of DXA-based structural engineering models of the proximal femur to discriminate hip fracture. J Bone Miner Res. 2009;24:33–42.CrossRefPubMed

29.

Karlamangla AS, Barrett-Connor E, Young J, Greendale GA. Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int. 2004;15:62–70.CrossRefPubMed

30.

Ishii S, Cauley JA, Crandall CJ, Srikanthan P, Greendale GA, Huang MH, et al. Diabetes and femoral neck strength: findings from The Hip Strength Across the Menopausal Transition Study. J Clin Endocrinol Metab. 2012;97:190–7.CrossRefPubMed

31.

Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, et al. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95:5045–55.CrossRefPubMed

32.

Yap SP, Baum T, Burghardt AJ, Link TM. Cortical porosity identifies fragility fractures in type-2 diabetic postmenopausal women. In European congress of radiology 2011, Book of Abstracts. 2011;S193.

33.

Shu A, Yin MT, Stein E, Cremers S, Dworakowski E, Ives R, et al. Bone structure and turnover in type 2 diabetes mellitus. Osteoporos Int. 2011 [Epub ahead of print].

34.

Nicks KM, Amin S, Atkinson EJ, Riggs BL, Melton LJ III, Khosla S. Relationship of age to bone microstructure independent of areal bone mineral density. J Bone Miner Res. 2011 [Epub ahead of print].

35.

Seeman E. Structural basis of growth-related gain and age-related loss of bone strength. Rheumatology (Oxford). 2008;47(Suppl 4):iv2–8.CrossRef

36.

Wang X, Puram S. The toughness of cortical bone and its relationship with age. Ann Biomed Eng. 2004;32:123–35.CrossRefPubMed

37.

Bell KL, Loveridge N, Power J, Garrahan N, Stanton M, Lunt M, et al. Structure of the femoral neck in hip fracture: cortical bone loss in the inferoanterior to superoposterior axis. J Bone Miner Res. 1999;14:111–9.CrossRefPubMed

38.

Ostertag A, Cohen-Solal M, Audran M, Legrand E, Marty C, Chappard D, et al. Vertebral fractures are associated with increased cortical porosity in iliac crest bone biopsy of men with idiopathic osteoporosis. Bone. 2009;44:413–7.CrossRefPubMed

39.

Goh SY, Cooper ME. Clinical review: the role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab. 2008;93:1143–52.CrossRefPubMed

40.

Paul RG, Bailey AJ. Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol. 1996;28:1297–310.CrossRefPubMed

41.

Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001;28:195–201.CrossRefPubMed

42.

Garnero P, Borel O, Gineyts E, Duboeuf F, Solberg H, Bouxsein ML, et al. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone. 2006;38:300–9.CrossRefPubMed

43.

Tang SY, Vashishth D. Non-enzymatic glycation alters microdamage formation in human cancellous bone. Bone. 2010;46:148–54.CrossRefPubMed

44.

Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. Bone. 2002;31:1–7.CrossRefPubMed

45.

Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, et al. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone. 2006;39:1073–9.CrossRefPubMed

46.

Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, et al. Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone. 2005;37:825–32.CrossRefPubMed

47.

Saito M, Fujii K, Marumo K. Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tissue Int. 2006;79:160–8.CrossRefPubMed

48.

Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, et al. Advanced glycation end products and bone loss during aging. Ann NY Acad Sci. 2005;1043:710–7.CrossRefPubMed

49.

Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T. Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. 2008;93:1013–9.CrossRefPubMed

50.

Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, et al. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab. 2009;94:2380–6.CrossRefPubMed

51.

Shiraki M, Kuroda T, Tanaka S, Saito M, Fukunaga M, Nakamura T. Nonenzymatic collagen cross-links induced by glycoxidation (pentosidine) predicts vertebral fractures. J Bone Miner Metab. 2008;26:93–100.CrossRefPubMed

52.

Gineyts E, Munoz F, Bertholon C, Sornay-Rendu E, Chapurlat R. Urinary levels of pentosidine and the risk of fracture in postmenopausal women: the OFELY study. Osteoporos Int. 2010;21:243–50.CrossRefPubMed

53.

Tang SY, Vashishth D. The relative contributions of non-enzymatic glycation and cortical porosity on the fracture toughness of aging bone. J Biomech. 2011;44:330–6.CrossRef

54.

Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. Bone loss and bone turnover in diabetes. Diabetes. 1995;44:775–82.CrossRefPubMed

55.

Armas LA, Akhter MP, Drincic A, Recker RR. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2011;50:91–6.CrossRefPubMed

56.

Suzuki K, Kurose T, Takizawa M, Maruyama M, Ushikawa K, Kikuyama M, et al. Osteoclastic function is accelerated in male patients with type 2 diabetes mellitus: the preventive role of osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG) on the decrease of bone mineral density. Diabetes Res Clin Pract. 2005;68:117–25.CrossRefPubMed

57.

Gerdhem P, Isaksson A, Akesson K, Obrant KJ. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int. 2005;16:1506–12.CrossRefPubMed

58.

Dobnig H, Piswanger-Solkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, et al. Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab. 2006;91:3355–63.CrossRefPubMed

59.

Achemlal L, Tellal S, Rkiouak F, Nouijai A, Bezza A, el Derouiche M, et al. Bone metabolism in male patients with type 2 diabetes. Clin Rheumatol. 2005;24:493–6.CrossRefPubMed

60.

Kindblom JM, Ohlsson C, Ljunggren O, Karlsson MK, Tivesten A, Smith U, et al. Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res. 2009;24:785–91.CrossRefPubMed

61.

Lin C, Jiang X, Dai Z, Guo X, Weng T, Wang J, et al. Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. J Bone Miner Res. 2009;24:1651–61.CrossRefPubMed

62.

Padhi D, Jang G, Stouch B, Fang L, Posvar E. Single-dose, placebo-controlled, randomized study of AMG 785, a sclerostin monoclonal antibody. J Bone Miner Res. 2011;26:19–26.CrossRefPubMed

63.

Arasu A, Cawthon P, Do T, Lui LY, Cauley J, Ensrud K, et al. Sclerostin and risk of hip fracture in older women. J Bone Miner Res. 2011;26:S143.CrossRef

64.

Garcia-Martin A, Rozas-Moreno P, Reyes-Garcia R, Morales-Santana S, Garcia-Fontana B, Garcia-Salcedo JA, et al. Circulating levels of sclerostin are increased in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2011;97:234–41.CrossRefPubMed

65.

Wehrli FW, Hopkins JA, Hwang SN, Song HK, Snyder PJ, Haddad JG. Cross-sectional study of osteopenia with quantitative MR imaging and bone densitometry. Radiology. 2000;217:527–38.PubMed

66.

Schellinger D, Lin CS, Hatipoglu HG, Fertikh D. Potential value of vertebral proton MR spectroscopy in determining bone weakness. AJNR Am J Neuroradiol. 2001;22:1620–7.PubMed

67.

Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, et al. Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology. 2005;236:945–51.CrossRefPubMed

68.

Griffith JF, Yeung DK, Antonio GE, Wong SY, Kwok TC, Woo J, et al. Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation. Radiology. 2006;241:831–8.CrossRefPubMed

69.

McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem. 2007;102:1343–57.CrossRefPubMed

70.

Rzonca SO, Suva LJ, Gaddy D, Montague DC, Lecka-Czernik B. Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology. 2004;145:401–6.CrossRefPubMed

71.

Sheu Y, Amati F, Schwartz A, Li X, Lee C, Gordon CL, et al. The relationship of bone marrow fat with bone geometry and strength differs by diabetic status. J Bone Miner Res. 2011;26. Available at http://www.asbmr.org/Meetings/AnnualMeeting/Abstract2011.aspx.

72.

Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM. Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Eurkaryotic Gene Expr. 2009;19:109–24.CrossRef

73.

Lecka-Czernik B. Marrow fat metabolism is linked to the systemic energy metabolism. Bone. 2012;50:534–9.CrossRefPubMed

74.

Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem. 2006;98:251–66.CrossRefPubMed

75.

Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell. 2004;3:379–89.CrossRefPubMed

76.

Rosen CJ, Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol. 2006;2:35–43.CrossRefPubMed

77.

Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000;21:115–37.CrossRefPubMed

78.

Rubin CT, Capilla E, Luu YK, Busa B, Crawford H, Nolan DJ, et al. Adipogenesis is inhibited by brief, daily exposure to high-frequency, extremely low-magnitude mechanical signals. Proc Natl Acad Sci USA. 2007;104:17879–84.CrossRefPubMed

79.

Payne MW, Uhthoff HK, Trudel G. Anemia of immobility: caused by adipocyte accumulation in bone marrow. Med Hypotheses. 2007;69:778–86.CrossRefPubMed

80.

David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, Jones DB, et al. Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology. 2007;148:2553–62.CrossRefPubMed

81.

Manolagas SC, Almeida M. Gone with the Wnts: {beta}-catenin, TCF, FOXO, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol. 2007;21:2605–14.CrossRefPubMed

82.

Sottile V, Seuwen K, Kneissel M. Enhanced marrow adipogenesis and bone resorption in estrogen-deprived rats treated with the PPARgamma agonist BRL49653 (rosiglitazone). Calcif Tissue Int. 2004;75:329–37.CrossRefPubMed

83.

Maurin AC, Chavassieux PM, Frappart L, Delmas PD, Serre CM, Meunier PJ. Influence of mature adipocytes on osteoblast proliferation in human primary cocultures. Bone. 2000;26:485–9.CrossRefPubMed

84.

Maurin AC, Chavassieux PM, Vericel E, Meunier PJ. Role of polyunsaturated fatty acids in the inhibitory effect of human adipocytes on osteoblastic proliferation. Bone. 2002;31:260–6.CrossRefPubMed

85.

Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112:1796–808.PubMed

86.

Rodriguez JP, Montecinos L, Rios S, Reyes P, Martinez J. Mesenchymal stem cells from osteoporotic patients produce a type I collagen-deficient extracellular matrix favoring adipogenic differentiation. J Cell Biochem. 2000;79:557–65.CrossRefPubMed

87.

Astudillo P, Rios S, Pastenes L, Pino AM, Rodriguez JP. Increased adipogenesis of osteoporotic human-mesenchymal stem cells (MSCs) characterizes by impaired leptin action. J Cell Biochem. 2008;103:1054–65.CrossRefPubMed

88.

Patel S, Hyer S, Tweed K, Kerry S, Allan K, Rodin A, et al. Risk factors for fractures and falls in older women with type 2 diabetes mellitus. Calcif Tissue Int. 2008;82:87–91.CrossRefPubMed

89.

Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif Tissue Int. 2007;80:353–8.CrossRefPubMed

90.

Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, et al. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA. 2011;305:2184–92.CrossRefPubMed

91.

World Health Organization. FRAX WHO fracture risk assessment tool. Access date: 2008; http://www.sheffield.ac.uk/FRAX/.

92.

Kanis JA, Oden A, Johnell O, Johansson H, De Laet C, Brown J, et al. The use of clinical risk factors enhances the performance of BMD in the prediction of hip and osteoporotic fractures in men and women. Osteoporos Int. 2007;18:1033–46.CrossRefPubMed

93.

Giangregorio L, Leslie W, Lix L, Johansson H, Oden A, McCloskey E, et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res. 2011 [Epub ahead of print].

94.

Holmberg AH, Nilsson PM, Nilsson JA, Akesson K. The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women. J Clin Endocrinol Metab. 2008;93:815–22.CrossRefPubMed

95.

Gagnon C, Magliano DJ, Ebeling PR, Dunstan DW, Zimmet PZ, Shaw JE, et al. Association between hyperglycaemia and fracture risk in non-diabetic middle-aged and older Australians: a national, population-based prospective study (AusDiab). Osteoporos Int. 2010;21:2067–74.CrossRefPubMed

96.

Ivers RQ, Cumming RG, Mitchell P, Peduto AJ. Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. 2001;24:1198–203.CrossRefPubMed

97.

Viegas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F. Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat. 2011;25:216–21.CrossRefPubMed

98.

Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yano S, Sugimoto T. Combination of obesity with hyperglycemia is a risk factor for the presence of vertebral fractures in type 2 diabetic men. Calcif Tissue Int. 2008;83:324–31.CrossRefPubMed

99.

Gregorio F, Cristallini S, Santeusanio F, Filipponi P, Fumelli P. Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract. 1994;23:43–54.CrossRefPubMed

100.

Schwartz AV, Vittinghoff E, Margolis KL, Ambrosius WT, Bonds DE, Josse RG, et al. Intensive glycemic control and fracture risk. Diabetes. 2011;60:A372.

101.

Schwartz AV, Vittinghoff E, Bonds DE, Hamilton BP, Ambrosius WT, Palermo L, et al. Intensive glycemic control not linked to falls in ACCORD. Diabetes. 2011;60:A372.

102.

Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRefPubMed

103.

Standards of medical care in diabetes—2009. Diabetes Care. 2009;32 Suppl 1:S13–S61.

104.

Kim JH, Jung MH, Lee JM, Son HS, Cha BY, Chang SA. Diabetic peripheral neuropathy is highly associated with non-traumatic fractures in Korean patients with type 2 diabetes mellitus. Clin Endocrinol (Oxf). 2011 [Epub ahead of print].

105.

Vestergaard P, Rejnmark L, Mosekilde L. Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int. 2009;84:45–55.CrossRefPubMed

106.

Shane E, Burr D, Ebeling PR, Abrahamsen B, Adler RA, Brown TD, et al. Atypical subtrochanteric and diaphyseal femoral fractures: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res. 2010;25:2267–94.CrossRefPubMed

107.

Black DM, Kelly MP, Genant HK, Palermo L, Eastell R, Bucci-Rechtweg C, et al. Bisphosphonates and fractures of the subtrochanteric or diaphyseal femur. N Engl J Med. 2010;362:1761–71.CrossRefPubMed

108.

Dagdelen S, Sener D, Bayraktar M. Influence of type 2 diabetes mellitus on bone mineral density response to bisphosphonates in late postmenopausal osteoporosis. Adv Ther. 2007;24:1314–20.CrossRefPubMed

109.

Iwamoto J, Sato Y, Uzawa M, Takeda T, Matsumoto H. Three-year experience with alendronate treatment in postmenopausal osteoporotic Japanese women with or without type 2 diabetes. Diabetes Res Clin Pract. 2011;93:166–73.CrossRefPubMed

110.

Saag KG, Zanchetta JR, Devogelaer JP, Adler RA, Eastell R, See K, et al. Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum. 2009;60:3346–55.CrossRefPubMed

Title: Clinical Aspects of Diabetic Bone Disease: An Update
Author: Ann V. Schwartz
Publication date: 01-03-2013
Publisher: Springer-Verlag
Published in: Clinical & Translational Metabolism / Issue 1/2013
Print ISSN: 1534-8644
Electronic ISSN: 2948-2445
DOI: https://doi.org/10.1007/s12018-012-9125-y

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