Bone and Diabetes

Starup-Linde, Jakob; Gregersen, Søren

doi:10.1007/978-3-319-44433-8_13

Jakob Starup-Linde⁵ &
Søren Gregersen⁵

Part of the book series: Endocrinology ((ENDOCR))

1450 Accesses
1 Citations

Abstract

Diabetes is associated with an increased risk of fracture. Commonly used risk factors underestimate the increased fracture risk, whereas they are solid predictors in subjects without diabetes. Bone mineral density measurements which are used for diagnosis of osteoporosis underestimate the fracture risk in patients with diabetes. Diabetes is a state of low bone turnover which may contribute to increased bone fragility. The low bone turnover is likely to be due to hyperglycemia and altered incretin response. Furthermore, diabetes may glycosylate bone collagen, which may reduce bone strength. Presently no specific treatment strategy is available for diabetes in regard of the bone. Although most anti-osteoporotic treatments seem to be safe, the benefit may be less when treating a low bone turnover disease. This chapter highlights the epidemiology, mechanisms, diagnosis, and treatment of diabetic bone disease.

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References

Abdalrahaman N, McComb C, Foster J, et al. Deficits in trabecular bone microarchitecture in young women with type 1 diabetes mellitus. J Bone Miner Res. 2015;30(8):1386–93. https://doi.org/10.1002/jbmr.2465.
Article CAS PubMed Google Scholar
Alba M, Xie J, Fung A, et al. The effects of canagliflozin, a sodium glucose co-transporter 2 inhibitor, on mineral metabolism and bone in patients with type 2 diabetes mellitus. Curr Med Res Opin. 2016;32(8):1375–85. https://doi.org/10.1080/03007995.2016.1174841.
Article CAS PubMed Google Scholar
American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2012;35(Suppl 1):S64–71. https://doi.org/10.2337/dc12-s064.
Article Google Scholar
Ardawi MS, Akhbar DH, Alshaikh A, et al. Increased serum sclerostin and decreased serum IGF-1 are associated with vertebral fractures among postmenopausal women with type-2 diabetes. Bone. 2013;56(2):355–62. https://doi.org/10.1016/j.bone.2013.06.029.
Article CAS PubMed Google Scholar
Armas LA, Akhter MP, Drincic A, et al. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2012;50(1):91–6. https://doi.org/10.1016/j.bone.2011.09.055.
Article PubMed Google Scholar
Basu R, Peterson J, Rizza R, et al. Effects of physiological variations in circulating insulin levels on bone turnover in humans. J Clin Endocrinol Metab. 2011;96(5):1450–5.
Article CAS PubMed PubMed Central Google Scholar
Bauer DC. HMG CoA reductase inhibitors and the skeleton: a comprehensive review. Osteoporos Int. 2003;14(4):273–82. https://doi.org/10.1007/s00198-002-1323-x.
Article CAS PubMed Google Scholar
Bjarnason NH, Henriksen EE, Alexandersen P, et al. Mechanism of circadian variation in bone resorption. Bone. 2002;30(1):307–13. https://doi.org/10.1016/S8756-3282(01)00662-7.
Article CAS PubMed Google Scholar
Bollag RJ, Zhong Q, Phillips P, et al. Osteoblast-derived cells express functional glucose-dependent insulinotropic peptide receptors. Endocrinology. 2000;141(3):1228–35. https://doi.org/10.1210/endo.141.3.7366.
Article CAS PubMed Google Scholar
Bonds DE, Larson JC, Schwartz AV, et al. Risk of fracture in women with type 2 diabetes: the women’s health initiative observational study. J Clin Endocrinol Metab. 2006;91(9):3404–10. https://doi.org/10.1210/jc.2006-0614.
Article CAS PubMed Google Scholar
Bone HG, Bolognese MA, Yuen CK, et al. Effects of denosumab treatment and discontinuation on bone mineral density and bone turnover markers in postmenopausal women with low bone mass. J Clin Endocrinol Metab. 2011;96(4):972–80. https://doi.org/10.1210/jc.2010-1502.
Article CAS PubMed Google Scholar
Bonewald LF. The amazing osteocyte. J Bone Miner Res. 2011;26(2):229–38. https://doi.org/10.1002/jbmr.320.
Article CAS PubMed Google Scholar
Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature. 2003;423(6937):337–42. https://doi.org/10.1038/nature01658.
Article CAS PubMed Google Scholar
Brunton SA. Nocturnal hypoglycemia: answering the challenge with long-acting insulin analogs. Med Gen Med. 2007;9(2):38.
Google Scholar
Canalis E, Mazziotti G, Giustina A, et al. Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int. 2007;18(10):1319–28. https://doi.org/10.1007/s00198-007-0394-0.
Article CAS PubMed Google Scholar
Carlsson S, Hammar N, Grill V, et al. Alcohol consumption and the incidence of type 2 diabetes: a 20-year follow-up of the finnish twin cohort study. Diabetes Care. 2003;26(10):2785–90.
Article PubMed Google Scholar
Chailurkit LO, Chanprasertyothin S, Rajatanavin R, et al. Reduced attenuation of bone resorption after oral glucose in type 2 diabetes. Clin Endocrinol. 2008;68(6):858–62. https://doi.org/10.1111/j.1365-2265.2007.03159.x.
Article CAS Google Scholar
Chapman IM. Obesity paradox during aging. Interdiscip Top Gerontol. 2010;37:20–36. https://doi.org/10.1159/000319992.
Article PubMed Google Scholar
Cheung AM, Adachi JD, Hanley DA, et al. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the Canadian bone strength working group. Curr Osteoporos Rep. 2013;11(2):136–46. https://doi.org/10.1007/s11914-013-0140-9.
Article PubMed PubMed Central Google Scholar
Clarke BL. Anti-sclerostin antibodies: utility in treatment of osteoporosis. Maturitas. 2014;78(3):199–204.
Article CAS PubMed Google Scholar
Clowes JA, Allen HC, Prentis DM, et al. Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab. 2003;88(10):4867–73. https://doi.org/10.1210/jc.2002-021447.
Article CAS PubMed Google Scholar
Colhoun HM, Livingstone SJ, Looker HC, et al. Hospitalised hip fracture risk with rosiglitazone and pioglitazone use compared with other glucose-lowering drugs. Diabetologia. 2012;55(11):2929–37. https://doi.org/10.1007/s00125-012-2668-0.
Article CAS PubMed PubMed Central Google Scholar
Compston J. Is fracture risk increased in patients with coeliac disease? Gut. 2003;52(4):459–60.
Article CAS PubMed PubMed Central Google Scholar
Conway BN, Long DM, Figaro MK, et al. Glycemic control and fracture risk in elderly patients with diabetes. Diabetes Res Clin Pract. 2016;115:47–53. https://doi.org/10.1016/j.diabres.2016.03.009.
Article PubMed PubMed Central Google Scholar
Dhaliwal R, Cibula D, Ghosh C, et al. Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int. 2014;25(7):1969–73. https://doi.org/10.1007/s00198-014-2704-7.
Article CAS PubMed Google Scholar
Driessen JH, van Onzenoort HA, Starup-Linde J, et al. Use of glucagon-like-peptide 1 receptor agonists and risk of fracture as compared to use of other anti-hyperglycemic drugs. Calcif Tissue Int. 2015a;97(5):506–15. https://doi.org/10.1007/s00223-015-0037-y.
Article CAS PubMed PubMed Central Google Scholar
Driessen JH, van Onzenoort HA, Starup-Linde J, et al. Use of dipeptidyl peptidase 4 inhibitors and fracture risk compared to use of other anti-hyperglycemic drugs. Pharmacoepidemiol Drug Saf. 2015b;24(10):1017–25. https://doi.org/10.1002/pds.3837.
Article CAS PubMed Google Scholar
Elbitar S, Khoury PE, Ghaleb Y, et al. Proprotein convertase subtilisin / kexin 9 (PCSK9) inhibitors and the future of dyslipidemia therapy: an updated patent review (2011-2015). Expert Opin Ther Pat. 2016;26(12):1377–92. https://doi.org/10.1080/13543776.2016.1206080.
Article CAS PubMed Google Scholar
Esser N, Legrand-Poels S, Piette J, et al. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract. 2014;105(2):141–50. https://doi.org/10.1016/j.diabres.2014.04.006.
Article CAS PubMed Google Scholar
Fan Y, Wei F, Lang Y, et al. Diabetes mellitus and risk of hip fractures: a meta-analysis. Osteoporos Int. 2015;27(1):219–28. https://doi.org/10.1007/s00198-015-3279-7.
Article CAS PubMed Google Scholar
Farr JN, Drake MT, Amin S, et al. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29(4):787–95. https://doi.org/10.1002/jbmr.2106.
Article PubMed Google Scholar
Ferrari S. Sequential/combined therapies in osteoporosis. Osteoporos Int. 2015;26(1):S65.
Google Scholar
Foy CG, Bell RA, Farmer DF, et al. Smoking and incidence of diabetes among U.S. adults: findings from the insulin resistance atherosclerosis study. Diabetes Care. 2005;28(10):2501–7. https://doi.org/10.2337/diacare.28.10.2501.
Article PubMed Google Scholar
Furst JR, Bandeira LC, Fan WW, et al. Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab. 2016;101(6):2502–10. https://doi.org/10.1210/jc.2016-1437.
Article CAS PubMed PubMed Central Google Scholar
Garcia-Hernandez A, Arzate H, Gil-Chavarria I, et al. High glucose concentrations alter the biomineralization process in human osteoblastic cells. Bone. 2012;50(1):276–88. https://doi.org/10.1016/j.bone.2011.10.032.
Article CAS PubMed Google Scholar
Giangregorio LM, Leslie WD, Lix LM, et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res. 2012;27(2):301–8. https://doi.org/10.1002/jbmr.556.
Article PubMed Google Scholar
Gimble JM, Zvonic S, Floyd ZE, et al. Playing with bone and fat. J Cell Biochem. 2006;98(2):251–66. https://doi.org/10.1002/jcb.20777.
Article CAS PubMed Google Scholar
Hall JE, Guyton AC. Guyton and hall textbook of medical physiology. 12th ed. Philadelphia: Saunders/Elsevier; 2011.
Google Scholar
Hardt PD, Brendel MD, Kloer HU, et al. Is pancreatic diabetes (type 3c diabetes) underdiagnosed and misdiagnosed? Diabetes Care. 2008;31(Suppl 2):S165–9. https://doi.org/10.2337/dc08-s244.
Article PubMed Google Scholar
Hasserius R, Karlsson MK, Jonsson B, et al. Long-term morbidity and mortality after a clinically diagnosed vertebral fracture in the elderly – a 12- and 22-year follow-up of 257 patients. Calcif Tissue Int. 2005;76(4):235–42. https://doi.org/10.1007/s00223-004-2222-2.
Article CAS PubMed Google Scholar
Heilmeier U, Cheng K, Pasco C, et al. Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporos Int. 2016;27(9):2791–802. https://doi.org/10.1007/s00198-016-3614-7.
Article CAS PubMed PubMed Central Google Scholar
Henriksen DB, Alexandersen P, Bjarnason NH, et al. Role of gastrointestinal hormones in postprandial reduction of bone resorption. J Bone Miner Res. 2003;18(12):2180–9. https://doi.org/10.1359/jbmr.2003.18.12.2180.
Article CAS PubMed Google Scholar
Hernandez JL, Olmos JM, Romana G, et al. Bone turnover markers in statin users: a population-based analysis from the Camargo cohort study. Maturitas. 2013;75(1):67–73. https://doi.org/10.1016/j.maturitas.2013.02.003.
Article CAS PubMed Google Scholar
Herrera A, Mateo J, Gil-Albarova J, et al. Prevalence of osteoporotic vertebral fracture in spanish women over age 45. Maturitas. 2015;80(3):288–95. https://doi.org/10.1016/j.maturitas.2014.12.004.
Article PubMed Google Scholar
Holst JJ, Knop FK, Vilsboll T, et al. Loss of incretin effect is a specific, important, and early characteristic of type 2 diabetes. Diabetes Care. 2011;34(Suppl 2):S251–7. https://doi.org/10.2337/dc11-s227.
Article CAS PubMed PubMed Central Google Scholar
Hwang JL, Weiss RE. Steroid-induced diabetes: a clinical and molecular approach to understanding and treatment. Diabetes Metab Res Rev. 2014;30(2):96–102. https://doi.org/10.1002/dmrr.2486.
Article CAS PubMed PubMed Central Google Scholar
Imai Y, Youn MY, Inoue K, et al. Nuclear receptors in bone physiology and diseases. Physiol Rev. 2013;93(2):481–523. https://doi.org/10.1152/physrev.00008.2012.
Article CAS PubMed PubMed Central Google Scholar
International Diabetes Federation. IDF diabetes atlas update. 2014. http://www.idf.org/diabetesatlas/update-2014. Accessed 10 Feb 2015
IOF. IOF epidemiology. 2015. http://www.iofbonehealth.org/epidemiology. Accessed 11 Feb 2015
Janghorbani M, van Dam RM, Willett WC, et al. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505. https://doi.org/10.1093/aje/kwm106.
Article PubMed Google Scholar
Kahn SE, Zinman B, Lachin JM, et al. Rosiglitazone-associated fractures in type 2 diabetes: an analysis from a diabetes outcome progression trial (ADOPT). Diabetes Care. 2008;31(5):845–51. https://doi.org/10.2337/dc07-2270.
Article CAS PubMed Google Scholar
Kanazawa I, Yamaguchi T, Sugimoto T. 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. 2011;22(4):1191–8. https://doi.org/10.1007/s00198-010-1310-6.
Article CAS PubMed Google Scholar
Kanis JA, Johansson H, Johnell O, et al. Alcohol intake as a risk factor for fracture. Osteoporos Int. 2005a;16(7):737–42. https://doi.org/10.1007/s00198-004-1734-y.
Article PubMed Google Scholar
Kanis JA, Johnell O, Oden A, et al. Smoking and fracture risk: a meta-analysis. Osteoporos Int. 2005b;16(2):155–62. https://doi.org/10.1007/s00198-004-1640-3.
Article CAS PubMed Google Scholar
Kannus P, Parkkari J, Niemi S, et al. Prevention of hip fracture in elderly people with use of a hip protector. N Engl J Med. 2000;343(21):1506–13. https://doi.org/10.1056/NEJM200011233432101.
Article CAS PubMed Google Scholar
Keegan TH, Schwartz AV, Bauer DC, et al. 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(7):1547–53. https://doi.org/10.2337/diacare.27.7.1547.
Article CAS PubMed Google Scholar
Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology. 2001;142(12):5050–5. https://doi.org/10.1210/endo.142.12.8536.
Article CAS PubMed Google Scholar
Khosla S, Riggs BL. Pathophysiology of age-related bone loss and osteoporosis. Endocrinol Metab Clin N Am. 2005;34(4):1015–30. https://doi.org/10.1016/j.ecl.2005.07.009.
Article CAS Google Scholar
Kim JH, Choi HJ, Ku EJ, et al. Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab. 2015;100(2):475–82. https://doi.org/10.1210/jc.2014-2047.
Article CAS PubMed Google Scholar
Kiyohara N, Yamamoto M, Sugimoto T. 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. 2015;10(12):e0144496. https://doi.org/10.1371/journal.pone.0144496.
Article CAS PubMed PubMed Central Google Scholar
Kostolanska J, Jakus V, Barak L. HbA1c and serum levels of advanced glycation and oxidation protein products in poorly and well controlled children and adolescents with type 1 diabetes mellitus. J Pediatr Endocrinol Metab. 2009;22(5):433–42.
Article CAS PubMed Google Scholar
Krakauer JC, McKenna MJ, Buderer NF, et al. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7):775–82.
Article CAS PubMed Google Scholar
Lapane KL, Yang S, Brown MJ, et al. Sulfonylureas and risk of falls and fractures: a systematic review. Drugs Aging. 2013;30(7):527–47. https://doi.org/10.1007/s40266-013-0081-0.
Article CAS PubMed Google Scholar
Lecka-Czernik B. PPARs in bone: the role in bone cell differentiation nd regulation of energy metabolism. Curr Osteoporosis Rep. 2010;8(2):84–90.
Article Google Scholar
Lecka-Czernik B, Rosen CJ, Kawai M. Skeletal aging and the adipocyte program: new insights from an “old” molecule. Cell Cycle. 2010;9(18):3648–54. https://doi.org/10.1111/j.1749-6632.2009.05221.x.
Article CAS PubMed PubMed Central Google Scholar
Lee RH, Colon-Emeric C. Increased fracture risk among women with diabetes mellitus is mediated by increased falls propensity. J Am Geriatr Soc. 2014;62:S58.
Google Scholar
Leslie WD, Aubry-Rozier B, Lamy O, et al. TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab. 2013;98(2):602–9. https://doi.org/10.1210/jc.2012-3118.
Article CAS PubMed Google Scholar
Leslie WD, Morin SN, Lix LM, et al. Does diabetes modify the effect of FRAX risk factors for predicting major osteoporotic and hip fracture? Osteoporos Int. 2014;25(12):2817–24. https://doi.org/10.1007/s00198-014-2822-2.
Article CAS PubMed Google Scholar
Li CI, Liu CS, Lin WY, et al. Glycated hemoglobin level and risk of hip fracture in older people with type 2 diabetes: a competing risk analysis of Taiwan diabetes cohort study. J Bone Miner Res. 2015;30(7):1338–46. https://doi.org/10.1002/jbmr.2462.
Article CAS PubMed Google Scholar
Luegmayr E, Glantschnig H, Wesolowski GA, et al. Osteoclast formation, survival and morphology are highly dependent on exogenous cholesterol/lipoproteins. Cell Death Differ. 2004;11(Suppl 1):S108–18. https://doi.org/10.1038/sj.cdd.4401399.
Article CAS PubMed Google Scholar
Mabilleau G, Mieczkowska A, Chappard D. Use of glucagon-like peptide-1 receptor agonists and bone fractures: a meta-analysis of randomized clinical trials. J Diabetes. 2014;6(3):260–6. https://doi.org/10.1111/1753-0407.12102.
Article CAS PubMed Google Scholar
Manavalan JS, Cremers S, Dempster DW, et al. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2012;97(9):3240–50. https://doi.org/10.1210/jc.2012-1546.
Article CAS PubMed PubMed Central Google Scholar
Martinez-Laguna D, Tebe C, Javaid MK, et al. Incident type 2 diabetes and hip fracture risk: a population-based matched cohort study. Osteoporos Int. 2015;26(2):827–33. https://doi.org/10.1007/s00198-014-2986-9.
Article CAS PubMed Google Scholar
McCarty MF. Anabolic effects of insulin on bone suggest a role for chromium picolinate in preservation of bone density. Med Hypotheses. 1995;45(3):241–6. https://doi.org/10.1016/0306-9877(95)90112-4.
Article CAS PubMed Google Scholar
Meier C, Schwartz AV, Egger A, et al. Effects of diabetes drugs on the skeleton. Bone. 2015;82:93–100. https://doi.org/10.1016/j.bone.2015.04.026.
Article CAS PubMed Google Scholar
Melton LJ III, Atkinson EJ, Cooper C, et al. Vertebral fractures predict subsequent fractures. Osteoporos Int. 1999;10(3):214–21. https://doi.org/10.1007/s001980050218.
Article PubMed Google Scholar
Melton LJ III, Leibson CL, Achenbach SJ, et al. Fracture risk in type 2 diabetes: update of a population-based study. J Bone Miner Res. 2008;23(8):1334–42. https://doi.org/10.1359/jbmr.080323.
Article PubMed PubMed Central Google Scholar
Monami M, Dicembrini I, Antenore A, et al. Dipeptidyl peptidase-4 inhibitors and bone fractures: a meta-analysis of randomized clinical trials. Diabetes Care. 2011;34(11):2474–6. https://doi.org/10.2337/dc11-1099.
Article PubMed PubMed Central Google Scholar
Munigala S, Agarwal B, Gelrud A, et al. Chronic pancreatitis and fracture: a retrospective, population-based veterans administration study. Pancreas. 2015;45(3):355–61. https://doi.org/10.1097/MPA.0000000000000381.
Article Google Scholar
Napoli N, Strotmeyer ES, Ensrud KE, et al. Fracture risk in diabetic elderly men: the MrOS study. Diabetologia. 2014;57(10):2057–65. https://doi.org/10.1007/s00125-014-3289-6.
Article CAS PubMed PubMed Central Google Scholar
Neumann T, Lodes S, Kastner B, et al. High serum pentosidine but not esRAGE is associated with prevalent fractures in type 1 diabetes independent of bone mineral density and glycaemic control. Osteoporos Int. 2014;25(5):1527–33. https://doi.org/10.1007/s00198-014-2631-7.
Article CAS PubMed Google Scholar
Nissen A, Christensen M, Knop FK, et al. Glucose-dependent insulinotropic polypeptide inhibits bone resorption in humans. J Clin Endocrinol Metab. 2014;99(11):E2325–9. https://doi.org/10.1210/jc.2014-2547.
Article CAS PubMed Google Scholar
Okayasu M, Nakayachi M, Hayashida C, et al. Low-density lipoprotein receptor deficiency causes impaired osteoclastogenesis and increased bone mass in mice because of defect in osteoclastic cell-cell fusion. J Biol Chem. 2012;287(23):19229–41. https://doi.org/10.1074/jbc.M111.323600.
Article CAS PubMed PubMed Central Google Scholar
Paccou J, Ward KA, Jameson KA, et al. Bone microarchitecture in men and women with diabetes: the importance of cortical porosity. Calcif Tissue Int. 2016;98(5):465–73. https://doi.org/10.1007/s00223-015-0100-8.
Article CAS PubMed Google Scholar
Pacheco-Pantoja EL, Ranganath LR, Gallagher JA, et al. Receptors and effects of gut hormones in three osteoblastic cell lines. BMC Physiol. 2011;11:12. https://doi.org/10.1186/1472-6793-11-12.
Article CAS PubMed PubMed Central Google Scholar
Palermo A, D’Onofrio L, Eastell R, et al. Oral anti-diabetic drugs and fracture risk, cut to the bone: safe or dangerous? A narrative review. Osteoporos Int. 2015;26(8):2073–89.
Article CAS PubMed Google Scholar
Panula J, Pihlajamaki H, Mattila VM, et al. Mortality and cause of death in hip fracture patients aged 65 or older: a population-based study. BMC Musculoskelet Disord. 2011;12:105. https://doi.org/10.1186/1471-2474-12-105.
Article PubMed PubMed Central Google Scholar
Patsch JM, Burghardt AJ, Yap SP, et al. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res. 2013;28(2):313–24. https://doi.org/10.1002/jbmr.1763.
Article PubMed Google Scholar
Pierce AM, Lindskog S, Hammarstrom L. Osteoclasts: structure and function. Electron Microsc Rev. 1991;4(1):1–45.
Article CAS PubMed Google Scholar
Pscherer S, Kostev K, Dippel FW, et al. Fracture risk in patients with type 2 diabetes under different antidiabetic treatment regimens: a retrospective database analysis in primary care. Diabetes Metab Syndr Obes. 2016;9:17–23. https://doi.org/10.2147/DMSO.S101370.
Article CAS PubMed PubMed Central Google Scholar
Rajpathak SN, Fu C, Brodovicz KG, et al. Sulfonylurea use and risk of hip fractures among elderly men and women with type 2 diabetes. Drugs Aging. 2015;32(4):321–7. https://doi.org/10.1007/s40266-015-0254-0.
Article CAS PubMed Google Scholar
Rejnmark L, Vestergaard P, Mosekilde L. Statin but not non-statin lipid-lowering drugs decrease fracture risk: a nation-wide case-control study. Calcif Tissue Int. 2006;79(1):27–36. https://doi.org/10.1007/s00223-006-0024-4.
Article CAS PubMed Google Scholar
Rubin MR, Paschalis EP, Poundarik A, et al. Advanced glycation endproducts and bone material properties in type 1 diabetic mice. PLoS One. 2016;11(5):e0154700. https://doi.org/10.1371/journal.pone.0154700.
Article CAS PubMed PubMed Central Google Scholar
Saito M, Kida Y, Kato S, et al. Diabetes, collagen, and bone quality. Curr Osteoporosis Rep. 2014;12(2):181–8.
Article Google Scholar
Santesso N, Carrasco-Labra A, Brignardello-Petersen R. Hip protectors for preventing hip fractures in older people. Cochrane Database Syst Rev. 2014;3:CD001255. https://doi.org/10.1002/14651858.CD001255.pub5.
Article Google Scholar
Sarles H. Chronic pancreatitis and diabetes. Bailliere Clin Endocrinol Metab. 1992;6(4):745–75.
Article CAS Google Scholar
Schwartz AV, Sellmeyer DE, Ensrud KE, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(1):32–8. https://doi.org/10.1210/jcem.86.1.7139.
Article CAS PubMed Google Scholar
Schwartz AV, Vittinghoff E, Bauer DC, et al. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA. 2011;305(21):2184–92. https://doi.org/10.1001/jama.2011.715.
Article CAS PubMed PubMed Central Google Scholar
Schwartz AV, Margolis KL, Sellmeyer DE, et al. Intensive glycemic control is not associated with fractures or falls in the ACCORD randomized trial. Diabetes Care. 2012;35(7):1525–31. https://doi.org/10.2337/dc11-2184.
Article PubMed PubMed Central Google Scholar
Schwartz AV, Pavo I, Alam J, et al. Teriparatide in patients with osteoporosis and type 2 diabetes. Bone. 2016;91:152–8. https://doi.org/10.1016/j.bone.2016.06.017.
Article CAS PubMed Google Scholar
Shah VN, Shah CS, Snell-Bergeon JK. Type 1 diabetes and risk of fracture: meta-analysis and review of the literature. Diabet Med. 2015;32(9):1134–42. https://doi.org/10.1111/dme.12734.
Article CAS PubMed PubMed Central Google Scholar
Shanbhogue VV, Hansen S, Frost M, et al. 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. 2015a;30(12):2188–99. https://doi.org/10.1002/jbmr.2573.
Article CAS PubMed Google Scholar
Shanbhogue VV, Hansen S, Frost M, et al. Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur J Endocrinol. 2015b;174(2):115–24. https://doi.org/10.1530/EJE-15-0860.
Article CAS PubMed Google Scholar
Shu A, Yin MT, Stein E, et al. Bone structure and turnover in type 2 diabetes mellitus. Osteoporos Int. 2012;23(2):635–41. https://doi.org/10.1007/s00198-011-1595-0.
Article CAS PubMed Google Scholar
Starup-Linde J. Investigations of diabetic bone disease: literature, registry, and clinical studies [Dissertation]. Aalborg: VBN, Aalborg University, The Faculty of Medicine, Department of Clinical Medicine (Videnbasen for Aalborg Universitet Aalborg Universitet, Det Sundhedsvidenskabelige Fakultet Klinisk Institute); 2015.
Google Scholar
Starup-Linde J, Vestergaard P. Biochemical bone turnover markers in diabetes mellitus - a systematic review. Bone. 2016;82:69–78. https://doi.org/10.1016/j.bone.2015.02.019.
Article CAS PubMed Google Scholar
Starup-Linde J, Eriksen SA, Lykkeboe S, et al. 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. 2014;25(6):1697–708.
Article CAS PubMed Google Scholar
Starup-Linde J, Frost M, Vestergaard P, et al. Epidemiology of fractures in diabetes. Calcif Tissue Int. 2016a;100(2):109–21. https://doi.org/10.1007/s00223-016-0175-x.
Article CAS PubMed Google Scholar
Starup-Linde J, Gregersen S, Vestergaard P. Associations with fracture in patients with diabetes: a nested case-control study. BMJ Open. 2016b;6(2):e009686. https://doi.org/10.1136/bmjopen-2015-009686.
Article PubMed PubMed Central Google Scholar
Starup-Linde J, Lykkeboe S, Gregersen S, et al. Bone structure and predictors of fracture in type 1 and type 2 diabetes. J Clin Endocrinol Metab. 2016c;101(3):928–36. https://doi.org/10.1210/jc.2015-3882.
Article CAS PubMed Google Scholar
Starup-Linde J, Lykkeboe S, Gregersen S, et al. Differences in biochemical bone markers by diabetes type and the impact of glucose. Bone. 2016d;83:149–55. https://doi.org/10.1016/j.bone.2015.11.004.
Article CAS PubMed Google Scholar
Tang X, Liu G, Kang J, et al. Obesity and risk of hip fracture in adults: a meta-analysis of prospective cohort studies. PLoS One. 2013;8(4):e55077. https://doi.org/10.1371/journal.pone.0055077.
Article CAS PubMed PubMed Central Google Scholar
Toh S, Hernandez-Diaz S. Statins and fracture risk. A systematic review. Pharmacoepidemiol Drug Saf. 2007;16(6):627–40. https://doi.org/10.1002/pds.1363.
Article CAS PubMed Google Scholar
Torekov SS, Iepsen EW, Lundgren J, et al. Treatment with a GLP-1 receptor agonist increases bone formation markers and prevents bone loss during weight loss maintenance in weight-reduced obese. Diabetes. 2015;64:A43.
Article Google Scholar
van Lierop AH, Hamdy NA, van der Meer RW, et al. Distinct effects of pioglitazone and metformin on circulating sclerostin and biochemical markers of bone turnover in men with type 2 diabetes mellitus. Eur J Endocrinol. 2012;166(4):711–6. https://doi.org/10.1530/EJE-11-1061.
Article CAS PubMed Google Scholar
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(4):427–44. https://doi.org/10.1007/s00198-006-0253-4.
Article CAS PubMed Google Scholar
Vestergaard P, Mosekilde L. Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid. 2002;12(5):411–9. https://doi.org/10.1089/105072502760043503.
Article PubMed Google Scholar
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(7):1292–9. https://doi.org/10.1007/s00125-005-1786-3.
Article CAS PubMed Google Scholar
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(1):45–55. https://doi.org/10.1007/s00223-008-9195-5.
Article CAS PubMed Google Scholar
Vestergaard P, Rejnmark L, Mosekilde L. Are antiresorptive drugs effective against fractures in patients with diabetes? Calcif Tissue Int. 2011;88(3):209–14.
Article CAS PubMed Google Scholar
Viegas M, Costa C, Lopes A, et al. 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(4):216–21. https://doi.org/10.1016/j.jdiacomp.2011.02.004.
Article Google Scholar
Waterloo S, Ahmed LA, Center JR, et al. Prevalence of vertebral fractures in women and men in the population-based tromso study. BMC Musculoskelet Disord. 2012;13:3. https://doi.org/10.1186/1471-2474-13-3.
Article PubMed PubMed Central Google Scholar
Weber DR, Haynes K, Leonard MB, et al. 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. 2015;38(10):1913–20. https://doi.org/10.2337/dc15-0783.
Article PubMed PubMed Central Google Scholar
Witek PR, Witek J, Pankowska E. Type 1 diabetes-associated autoimmune diseases: screening, diagnostic principles and management. Med Wieku Rozwoj. 2012;16(1):23–34.
PubMed Google Scholar
Xie D, Cheng H, Hamrick M, et al. Glucose-dependent insulinotropic polypeptide receptor knockout mice have altered bone turnover. Bone. 2005;37(6):759–69. https://doi.org/10.1016/j.bone.2005.06.021.
Article CAS PubMed Google Scholar
Xie D, Zhong Q, Ding KH, et al. Glucose-dependent insulinotropic peptide-overexpressing transgenic mice have increased bone mass. Bone. 2007;40(5):1352–60. https://doi.org/10.1016/j.bone.2007.01.007.
Article CAS PubMed Google Scholar
Xu J, Yue F, Wang J, et al. High glucose inhibits receptor activator of nuclear factorÎ°B ligand-induced osteoclast differentiation via downregulation of vATPase V0 subunit d2 and dendritic cellspecific transmembrane protein. Mol Med Rep. 2014;11(2):865–70.
Article PubMed PubMed Central Google Scholar
Xu J, Yue F, Wang J, et al. High glucose inhibits receptor activator of nuclear factorkappaB ligand-induced osteoclast differentiation via downregulation of vATPase V0 subunit d2 and dendritic cellspecific transmembrane protein. Mol Med Rep. 2015;11(2):865–70. https://doi.org/10.3892/mmr.2014.2807.
Article CAS PubMed Google Scholar
Yamamoto M, Yamauchi M, Sugimoto T. Elevated sclerostin levels are associated with vertebral fractures in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2013;98(10):4030–7. https://doi.org/10.1210/jc.2013-2143.
Article CAS PubMed Google Scholar
Yang X, Mostafa AJ, Appleford M, et al. Bone formation is affected by matrix advanced glycation end products (AGEs) in vivo. Calcif Tissue Int. 2016;99(4):373–83. https://doi.org/10.1007/s00223-016-0153-3.
Article CAS PubMed Google Scholar
Zhong Q, Itokawa T, Sridhar S, et al. Effects of glucose-dependent insulinotropic peptide on osteoclast function. Am J Physiol Endocrinol Metab. 2007;292(2):E543–8. https://doi.org/10.1152/ajpendo.00364.2006.
Article CAS PubMed Google Scholar

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Department of Endocrinology and Internal Medicine, Aarhus University Hospital, Aarhus, Denmark
Jakob Starup-Linde & Søren Gregersen

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Jakob Starup-Linde
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Søren Gregersen
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Correspondence to Jakob Starup-Linde .

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Division of Endocrinology, Diabetes and Metabolism, University and Hospital Trust of Verona, Verona, Italy
Enzo Bonora
Diabetes Division, Diabetes Research Unit, University of Texas Health Science Center, San Antonio, TX, USA
Ralph A. DeFronzo

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Starup-Linde, J., Gregersen, S. (2018). Bone and Diabetes. In: Bonora, E., DeFronzo, R. (eds) Diabetes Complications, Comorbidities and Related Disorders. Endocrinology. Springer, Cham. https://doi.org/10.1007/978-3-319-44433-8_13

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DOI: https://doi.org/10.1007/978-3-319-44433-8_13
Published: 12 October 2018
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-44432-1
Online ISBN: 978-3-319-44433-8
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