Bone Metabolism and Fracture Risk in Diabetes Mellitus
Keywords:
bone metabolism, diabetes mellitus, bone remodeling, biomarkersAbstract
Individuals with type 1 diabetes mellitus (T1DM) and type 2 diabetes mellitus (T2DM) are at increased risk for fragility fractures. Bone mineral density (BMD) is decreased in T1DM but often normal or even elevated in T2DM when compared with age-matched non-DM populations. However, bone turnover is decreased in both T1DM and T2DM. The pathophysiologic mechanisms leading to bone fragility is multifactorial, and potentially leads to reduced bone formation, altered bone microstructure and decreased bone strength. Interestingly, different antidiabetic treatments may influence fracture risk due to effects on glycemic control, triggering of hypoglycemic events or osteoblastogenesis.
Downloads
References
International Diabetes Federation. IDF Diabetes Atlas, 7th ed, 2015.
Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495-505. PMID: 17575306. https://doi.org/10.1093/aje/kwm106.
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(7):1573-8. PMID: 16801581. https://doi.org/10.2337/dc06-0440.
Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res. 2009;24(4):702-9. PMID: 19049338. https://doi.org/10.1359/jbmr.081207.
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. PMID: 17068657. https://doi.org/10.1007/s00198-006-0253-4.
Burghardt AJ, Issever AS, Schwartz AV, 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(11):5045-55. PMID: 20719835. PMCID: PMC2968722. https://doi.org/10.1210/jc.2010-0226.
Farr JN, Drake MT, Amin S, Melton LJ 3rd, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29(4):787-95. PMID: 24123088. PMCID: PMC3961509. https://doi.org/10.1002/jbmr.2106.
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. PMID: 22991256. PMCID: PMC3534818. https://doi.org/10.1002/jbmr.1763.
Shanbhogue VV, Hansen S, Frost M, et al. Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur J Endocrinol. 2016;174(2):115-24. PMID: 26537860. https://doi.org/10.1530/EJE-15-0860.
Muñoz-Torres M, Jódar E, Escobar-Jiménez F, López-Ibarra PJ, Luna JD. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int. 1996;58(5):316-9. PMID: 8661964.
Miazgowski T, Czekalski S. 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. 1998;8(5):399-403. PMID: 9850345. https://doi.org/10.1007/s001980050082.
Jehle PM, Jehle DR, Mohan S, Böhm BO. Serum levels of insulin-like growth factor system components and relationship to bone metabolism in type 1 and type 2 diabetes mellitus patients. J Endocrinol. 1998;159(2):297-306. PMID: 9795371.
Tuominen JT, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22(7):1196-200. PMID: 10388989.
Gallacher SJ, Fenner JA, Fisher BM, et al. An evaluation of bone density and turnover in premenopausal women with type 1 diabetes mellitus. Diabet Med. 1993;10(2):129-33. PMID: 8096168.
Weber G, Beccaria L, de'Angelis M, et al. Bone mass in young patients with type I diabetes. Bone Miner. 1990;8(1):23-30. PMID: 2306551.
Cummings SR, Nevitt MC, Browner WS, et al. Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N Engl J Med. 1995;332(12):767-73. PMID: 7862179. https://doi.org/10.1056/NEJM199503233321202.
Ivers RQ, Cumming RG, Mitchell P, Peduto AJ; Blue Mountains Eye Study. Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. 2001;24(7):1198-203. PMID: 11423502.
Nicodemus KK, Folsom AR; Iowa Women's Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24(7):1192-7. PMID: 11423501.
Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T. Bone mineral density measured by dual energy x-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone. 1993;14(1):29-33. PMID: 8442999.
van Daele PL, Stolk RP, Burger H, et al. Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med. 1995;122(6):409-14. PMID: 7856988.
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. PMID: 11231974. https://doi.org/10.1210/jcem.86.1.7139.
Hadjidakis DJ, Androulakis II. Bone remodeling. Ann N Y Acad Sci. 2006;1092:385-96. PMID: 17308163. https://doi.org/10.1196/annals.1365.035.
Taylor AK, Lueken SA, Libanati C, Baylink DJ. Biochemical markers of bone turnover for the clinical assessment of bone metabolism. Rheum Dis Clin North Am. 1994;20(3):589-607. PMID: 7984780.
McKee MD, Nanci A. Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: Ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech. 1996;33(2):141-64. PMID: 8845514.
Hanson DA, Weis MA, Bollen AM, Maslan SL, Singer FR, Eyre DR. A specific immunoassay for monitoring human bone resorption: Quantitation of type I collagen cross‐linked N‐telopeptides in urine. J Bone Miner Res. 1992;7(11):1251-8. PMID: 1466251.
Christgau S, Rosenquist C, Alexandersen P, et al. Clinical evaluation of the Serum CrossLaps One Step ELISA, a new assay measuring the serum concentration of bone-derived degradation products of type I collagen C-telopeptides. Clin Chem. 1998;44(11):2290-300. PMID: 9799756.
Fink E, Cormier C, Steinmetz P, Kindermans C, Le Bouc Y, Souberbielle JC. Differences in the capacity of several biochemical bone markers to assess high bone turnover in early menopause and response to alendronate therapy. Osteoporos Int. 2000;11(4):295-303. PMID: 10928218. https://doi.org/ 10.1007/PL00004183.
Hannon R, Blumsohn A, Naylor K, Eastell R. Response of biochemical markers of bone turnover to hormone replacement therapy: Impact of biological variability. J Bone Miner Res. 1998;13(7):1124-33. PMID: 9661076. https://doi.org/10.1359/jbmr.1998.13.7.1124.
Seibel MJ. Biochemical markers of bone turnover part I: Biochemistry and variability. Clin Biochem Rev. 2005;26(4):97-122. PMID: 16648882. PMCID: PMC1320175.
Forst T, Beyer J, Pfützner A, et al. Peripheral osteopenia in adult patients with insulin‐dependent diabetes mellitus. Diabet Med. 1995;12(10):874-9. PMID: 8846677.
Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest. 2000;23(5):295-303. PMID: 10882147. https://doi.org/10.1007/BF03343726.
Hadjidakis DJ, Raptis AE, Sfakianakis M, Mylonakis A, Raptis SA. Bone mineral density of both genders in type 1 diabetes according to bone composition. J Diabetes Complications. 2006;20(5):302-7. PMID: 16949517. https://doi.org/10.1016/j.jdiacomp.2005.07.006.
Strotmeyer ES, Cauley JA, Orchard TJ, Steenkiste AR, Dorman JS. Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes Care. 2006;29(2):306-11. PMID: 16443878.
Mastrandrea LD, Wactawski-Wende J, Donahue RP, Hovey KM, Clark A, Quattrin T. Young women with type 1 diabetes have lower bone mineral density that persists over time. Diabetes Care. 2008;31(9):1729-35. PMID: 18591404. PMCID: PMC2518333. https://doi.org/10.2337/dc07-2426.
Campos Pastor MM, López-Ibarra PJ, Escobar-Jiménez F, Serrano Pardo M, García-Cervigón AG. Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: A prospective study. Osteoporos Int. 2000;11(5):455-9. PMID: 10912849.
Eller-Vainicher C, Zhukouskaya VV, Tolkachev YV, et al. Low bone mineral density and its predictors in type 1 diabetic patients evaluated by the classic statistics and artificial neural network analysis. Diabetes Care. 2011;34(10):2186-91. PMID: 21852680. PMCID: PMC3177712. https://doi.org/10.2337/dc11-0764.
Joshi A, Varthakavi P, Chadha M, Bhagwat N. A study of bone mineral density and its determinants in type 1 diabetes mellitus. J Osteoporos. 2013;2013:397814. PMID: 23607045. PMCID: PMC3628496. https://doi.org/10.1155/2013/397814.
Soto N, Pruzzo R, Eyzaguirre F, et al. Bone mass and sex steroids in postmenarcheal adolescents and adult women with type 1 diabetes mellitus. J Diabetes Complications. 2011;25(1):19-24. PMID: 19955005. https://doi.org/10.1016/j.jdiacomp.2009.10.002.
Bechtold S, Dirlenbach I, Raile K, Noelle V, Bonfig W, Schwarz HP. Early manifestation of type 1 diabetes in children is a risk factor for changed bone geometry: Data using peripheral quantitative computed tomography. Pediatrics. 2006;118(3):e627-34. PMID: 16908617. https://doi.org/10.1542/peds.2005-2193.
Danielson KK, Elliott ME, LeCaire T, Binkley N, Palta M. Poor glycemic control is associated with low BMD detected in premenopausal women with type 1 diabetes. Osteoporos Int. 2009;20(6):923-33. PMID: 18830554. PMCID: PMC2748939. https://doi.org/10.1007/s00198-008-0763-3.
Heap J, Murray MA, Miller SC, Jalili T, Moyer-Mileur LJ. Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr. 2004;144(1):56-62. PMID: 14722519. https://doi.org/10.1016/j.jpeds.2003.10.066.
Lettgen B, Hauffa B, Möhlmann C, Jeken C, Reiners C. 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. 1995;43(5):173-5. PMID: 7782045.
Saha MT, Sievänen H, Salo MK, Tulokas S, Saha HH. Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int. 2009;20(8):1401-6. PMID: 19083073. https://doi.org/10.1007/s00198-008-0810-0.
Forsén L, Meyer H, Midthjell K, Edna TH. Diabetes mellitus and the incidence of hip fracture: Results from the Nord-Trøndelag Health Survey. Diabetologia. 1999;42(8):920-5. PMID: 10491750. https://doi.org/10.1007/s001250051248.
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(4):495-500. PMID: 16283065. https://doi.org/10.1007/s00198-005-0013-x.
Napoli N, Strotmeyer ES, Ensrud KE, et al. Fracture risk in diabetic elderly men: The MrOS study. Diabetologia. 2014;57(10):2057-65. PMID: 24908567. PMCID: PMC4344350. https://doi.org/10.1007/s00125-014-3289-6.
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. PMID: 25598134. https://doi.org/10.1002/jbmr.2462.
Johnston S, Conner C, Aagren M, Ruiz K, Bouchard J. Association between hypoglycaemic events and fall‐related fractures in Medicare‐covered patients with type 2 diabetes. Diabetes Obes Metab. 2012;14(7):634-43. PMID: 22335246. https://doi.org/10.1111/j.1463-1326.2012.01583.x.
de Liefde II, 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(12):1713-20. PMID: 15940395. https://doi.org/10.1007/s00198-005-1909-1.
Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, et al. Risk of fracture in women with type 2 diabetes: The Women’s Health Initiat.ive Observational Study. J Clin Endocrinol Metab. 2006;91(9):3404-10. PMID: 16804043. https://doi.org/10.1210/jc.2006-0614.
Kwon DJ, Kim JH, Chung KW, et al. Bone mineral density of the spine using dual energy x‐ray absorptiometry in patients with non‐insulin‐dependent diabetes mellitus. J Obstet Gynaecol Res. 1996;22(2):157-62. PMID: 8697346.
Pérez-Castrillón JL, De Luis D, Martín-Escudero JC, Asensio T, del Amo R, Izaola O. Non-insulin-dependent diabetes, bone mineral density, and cardiovascular risk factors. J Diabetes Complications. 2004;18(6):317-21. PMID: 15531180. https://doi.org/10.1016/S1056-8727(03)00072-2.
Lunt M, Masaryk P, Scheidt-Nave C, et al. The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: The EVOS study. Osteoporos Int. 2001;12(8):688-98. PMID: 11580083.
Hanley D, Brown J, Tenenhouse A, et al. Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: Cross‐sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res. 2003;18(4):784-90. PMID: 12674340. https://doi.org/10.1359/jbmr.2003.18.4.784.
Dennison E, Syddall H, Sayer AA, Craighead S, Phillips D, Cooper C. 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. 2004;47(11):1963-8. PMID: 15565368. https://doi.org/10.1007/s00125-004-1560-y.
Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non—insulin-dependent diabetes mellitus. JAMA. 1992;268(23):3333-7. PMID: 1453525.
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(12):1506-12. PMID: 15824889. https://doi.org/10.1007/s00198-005-1877-5.
Schwartz AV, Sellmeyer DE, Strotmeyer ES, et al. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res. 2005;20(4):596-603. PMID: 15765178. https://doi.org/10.1359/JBMR.041219.
Dobnig H, Piswanger-Solkner JC, Roth M, 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(9):3355-63. PMID: 16735485. https://doi.org/10.1210/jc.2006-0460.
Strotmeyer ES, Cauley JA, Schwartz AV, et al. Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: The Health, Aging, and Body Composition Study. J Bone Miner Res. 2004;19(7):1084-91. PMID: 15176990. https://doi.org/ 10.1359/JBMR.040311.
Pritchard JM, Giangregorio LM, Atkinson SA, et al. Changes in trabecular bone microarchitecture in postmenopausal women with and without type 2 diabetes: A two year longitudinal study. BMC Musculoskelet Disord. 2013;14:114. PMID: 23530948. PMCID: PMC3618189. https://doi.org/10.1186/1471-2474-14-114.
Pritchard JM, Giangregorio LM, Atkinson SA, et al. Association of larger holes in the trabecular bone at the distal radius in postmenopausal women with type 2 diabetes mellitus compared to controls. Arthritis Care Res (Hoboken). 2012;64(1):83-91. PMID: 22213724. PMCID: PMC5096917. https://doi.org/10.1002/acr.20602.
Randall C, Bridges D, Guerri R, et al. Applications of a new handheld reference point indentation instrument measuring bone material strength. J Med Device. 2013;7(4):0410051-6. PMID: 24115973. PMCID: PMC3792445. https://doi.org/ 10.1115/1.4024829.
Dubey A, Aharonoff GB, Zuckerman JD, Koval KJ. The effects of diabetes on outcome after hip fracture. Bull Hosp Jt Dis. 2000;59(2):94-8. PMID: 10983258.
Huang YF, Shyu YI, Liang J, Chen MC, Cheng HS, Wu CC. Diabetes and health outcomes among older Taiwanese with hip fracture. Rejuvenation Res. 2012;15(5):476-82. PMID: 22998328. https://doi.org/10.1089/rej.2011.1308.
Muraki S, Yamamoto S, Ishibashi H, Nakamura K. Factors associated with mortality following hip fracture in Japan. J Bone Miner Metab. 2006;24(2):100-4. PMID: 16502115. https://doi.org/10.1007/s00774-005-0654-z.
Napoli N, Chandran M, Pierroz DD, et al. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. 2017;13(4):208-19. PMID: 27658727. https://doi.org/10.1038/nrendo.2016.153.
Hough FS, Pierroz DD, Cooper C, Ferrari SL; IOF CSA Bone and Diabetes Working Group. Mechanisms in endocrinology: Mechanisms and evaluation of bone fragility in type 1 diabetes mellitus. Eur J Endocrinol. 2016;174(4):R127-38. PMID: 26537861. https://doi.org/10.1530/EJE-15-0820.
Napoli N, Strollo R, Paladini A, Briganti SI, Pozzilli P, Epstein S. The alliance of mesenchymal stem cells, bone, and diabetes. Int J Endocrinol. 2014;2014:690783. PMID: 25140176. PMCID: PMC4124651. https://doi.org/ 10.1155/2014/690783.
Maggio AB, Ferrari S, Kraenzlin M, et al. Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. J Pediatr Endocrinol Metab. 2010;23(7):697-707. PMID: 20857842.
Adami S. Bone health in diabetes: Considerations for clinical management. Curr Med Res Opin. 2009;25(5):1057-72. PMID: 19292601. https://doi.org/ 10.1185/03007990902801147.
Díaz-López A, Bulló M, Juanola-Falgarona M, et al. Reduced serum concentrations of carboxylated and undercarboxylated osteocalcin are associated with risk of developing type 2 diabetes mellitus in a high cardiovascular risk population: A nested case-control study. J Clin Endocrinol Metab. 2013;98(11):4524-31. PMID: 24037881. https://doi.org/10.1210/jc.2013-2472.
Starup-Linde J, Eriksen SA, Lykkeboe S, Handberg A, Vestergaard P. 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. PMID: 24676844. https://doi.org/10.1007/s00198-014-2676-7.
Leite Duarte ME, da Silva RD. Histomorphometric analysis of the bone tissue in patients with non-insulin-dependent diabetes (DMNID). Rev Hosp Clin Fac Med Sao Paulo. 1995;51(1):7-11. PMID: 8762647.
Weyer C, Funahashi T, Tanaka S, et al. Hypoadiponectinemia in obesity and type 2 diabetes: Close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab. 2001;86(5):1930-5. PMID: 11344187. https://doi.org/ 10.1210/jcem.86.5.7463.
Williams GA, Wang Y, Callon KE, et al. In vitro and in vivo effects of adiponectin on bone. Endocrinology. 2009;150(8):3603-10. PMID: 19406946. https://doi.org/10.1210/en.2008-1639.
Tamura T, Yoneda M, Yamane K, et al. Serum leptin and adiponectin are positively associated with bone mineral density at the distal radius in patients with type 2 diabetes mellitus. Metabolism. 2007;56(5):623-8. PMID: 17445536. https://doi.org/10.1016/j.metabol.2006.12.008.
Wang W, Zhang X, Zheng J, Yang J. High glucose stimulates adipogenic and inhibits osteogenic differentiation in MG-63 cells through cAMP/protein kinase A/extracellular signal-regulated kinase pathway. Mol Cell Biochem. 2010;338(1-2):115-22. PMID: 19949837. https://doi.org/10.1007/s11010-009-0344-6.
Botolin S, Faugere MC, Malluche H, Orth M, Meyer R, McCabe LR. Increased bone adiposity and peroxisomal proliferator-activated receptor-gamma2 expression in type I diabetic mice. Endocrinology. 2005;146(8):3622-31. PMID: 15905321. PMCID: PMC1242186. https://doi.org/10.1210/en.2004-1677.
Bucala R, Vlassara H. Advanced glycosylation end products in diabetic renal and vascular disease. Am J Kidney Dis. 1995;26(6):875-88. PMID: 7503061.
Gefter JV, Shaufl AL, Fink MP, Delude RL. Comparison of distinct protein isoforms of the receptor for advanced glycation end-products expressed in murine tissues and cell lines. Cell Tissue Res. 2009;337(1):79-89. PMID: 19415334. https://doi.org/10.1007/s00441-009-0791-0.
Ramasamy R, Yan SF, Schmidt AM. Advanced glycation endproducts: From precursors to RAGE: Round and round we go. Amino Acids. 2012;42(4):1151-61. PMID: 20957395. PMCID: PMC3062728. https://doi.org/10.1007/s00726-010-0773-2.
Odetti P, Rossi S, Monacelli F, et al. Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci. 2005;1043:710-7. PMID: 16037297. https://doi.org/10.1196/annals.1333.082.
Hein GE. Glycation endproducts in osteoporosis—is there a pathophysiologic importance? Clin Chim Acta. 2006;371(1-2):32-6. PMID: 16777084. https://doi.org/10.1016/j.cca.2006.03.017.
Dong XN, Qin A, Xu J, Wang X. In situ accumulation of advanced glycation endproducts (AGEs) in bone matrix and its correlation with osteoclastic bone resorption. Bone. 2011;49(2):174-83. PMID: 21530698. PMCID: PMC3117937. https://doi.org/10.1016/j.bone.2011.04.009.
Tang S, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone. 2007;40(4):1144-51. PMID: 17257914. PMCID: PMC4398019. https://doi.org/10.1016/j.bone.2006.12.056.
Sanguineti R, Storace D, Monacelli F, Federici A, Odetti P. Pentosidine effects on human osteoblastsin vitro. Ann N Y Acad Sci. 2008;1126:166-72. PMID: 18448811. https://doi.org/10.1196/annals.1433.044.
Yang J, Zhang X, Wang W, Liu J. Insulin stimulates osteoblast proliferation and differentiation through ERK and PI3K in MG‐63 cells. Cell Biochem Funct. 2010;28(4):334-41. PMID: 20517899. https://doi.org/10.1002/cbf.1668.
Gandhi A, Beam HA, O'Connor JP, Parsons JR, Lin SS. The effects of local insulin delivery on diabetic fracture healing. Bone. 2005;37(4):482-90. PMID: 16027060. https://doi.org/10.1016/j.bone.2005.04.039.
McCarthy AD, Etcheverry SB, Cortizo AM. Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: Role in osteoblast development. Acta Diabetol. 2001;38(3):113-22. PMID: 11827431.
Terada M, Inaba M, Yano Y, et al. Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone. 1998;22(1):17-23. PMID: 9437509.
Gilbert L, He X, Farmer P, et al. Inhibition of osteoblast differentiation by tumor necrosis factor-α 1. Endocrinology. 2000;141(11):3956-64. PMID: 11089525. https://doi.org/10.1210/endo.141.11.7739.
Glantschnig H, Fisher JE, Wesolowski G, Rodan GA, Reszka AA. M-CSF, TNFα and RANK ligand promote osteoclast survival by signaling through mTOR/S6 kinase. Cell Death Differ. 2003;10(10):1165-77. PMID: 14502240. https://doi.org/10.1038/sj.cdd.4401285.
Stratton IM, Adler AI, Neil HAW, et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): Prospective observational study. BMJ. 2000;321(7258):405-12. PMID: 10938048. PMCID: PMC27454.
Oei L, Zillikens MC, Dehghan A, Buitendijk GH, et al. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: The Rotterdam Study. Diabetes Care. 2013;36(6):1619-28. PMID: 23315602. PMCID: PMC3661786. https://doi.org/10.2337/dc12-1188.
Schneider AL, Williams EK, Brancati FL, Blecker S, Coresh J, Selvin E. Diabetes and risk of fracture-related hospitalization: The atherosclerosis risk in communities study. Diabetes Care. 2013;36(5):1153-8. PMID: 23248194. PMCID: PMC3631877. https://doi.org/10.2337/dc12-1168.
Schwartz AV, Vittinghoff E, Sellmeyer DE, et al. Diabetes-related complications, glycemic control, and falls in older adults. Diabetes Care. 2008;31(3):391-6. PMID: 18056893. PMCID: PMC2288549. https://doi.org/10.2337/dc07-1152.
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. PMID: 15909154. https://doi.org/10.1007/s00125-005-1786-3.
Solomon DH, Cadarette SM, Choudhry NK, Canning C, Levin R, Stürmer T. A cohort study of thiazolidinediones and fractures in older adults with diabetes. J Clin Endocrinol Metab. 2009;94(8):2792-8. PMID: 19470635 PMCID: PMC2730861. https://doi.org/10.1210/jc.2008-2157.
Del Prato S, Camisasca R, Wilson C, Fleck P. Durability of the efficacy and safety of alogliptin compared with glipizide in type 2 diabetes mellitus: A 2‐year study. Diabetes Obes Metab. 2014;16(12):1239-46. PMID: 25132212. https://doi.org/10.1111/dom.12377.
Loke YK, Singh S, Furberg CD. Long-term use of thiazolidinediones and fractures in type 2 diabetes: a meta-analysis. Can Med Assoc J. 2009;180(1):32-9. PMID: 1907365. PMCID: PMC2612065. https://doi.org/10.1503/cmaj.080486.
Zhu ZN, Jiang YF, Ding T. Risk of fracture with thiazolidinediones: An updated meta-analysis of randomized clinical trials. Bone. 2014;68:115-23. PMID: 25173606. https://doi.org/10.1016/j.bone.2014.08.010.
Su B, Sheng H, Zhang M, et al. Risk of bone fractures associated with glucagon-like peptide-1 receptor agonists’ treatment: A meta-analysis of randomized controlled trials. Endocrine. 2015;48(1):107-15. PMID: 25074632. https://doi.org/10.1007/s12020-014-0361-4.
Monami M, Dicembrini I, Antenore A, Mannucci E. Dipeptidyl peptidase-4 inhibitors and bone fractures: A Meta-analysis of randomized clinical trials. Diabetes Care 2011 34(11): 2474–6. PMID: 22025784. PMCID: PMC3198283. https://doi.org/10.2337/dc11-1099.
Mosenzon O, Wei C, Davidson J, et al. Incidence of fractures in patients with type 2 diabetes in the SAVOR-TIMI 53 trial. Diabetes Care. 2015;38(11):2142-50. PMID: 26358285. https://doi.org/10.2337/dc15-1068.
DeFronzo R, Davidson J, Del Prato S. The role of the kidneys in glucose homeostasis: A new path towards normalizing glycaemia. Diabetes Obes Metab. 2012;14(1):5-14. PMID: 21955459. https://doi.org/10.1111/j.1463-1326.2011.01511.x.
Bilezikian JP, Watts NB, Usiskin K, et al. Evaluation of bone mineral density and bone biomarkers in patients with type 2 diabetes treated with canagliflozin. J Clin Endocrinol Metab. 2015;101(1):44-51. PMID: 26580234. PMCID: PMC4701848. https://doi.org/10.1210/jc.2015-1860.
Watts NB, Bilezikian JP, Usiskin K, et al. Effects of canagliflozin on fracture risk in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2015;101(1):157-66. PMID: 26580237. PMCID: PMC4701850. https://doi.org/10.1210/jc.2015-3167.
Vasikaran S, Eastell R, Bruyère O, et al. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: A need for international reference standards. Osteoporos Int. 2011;22(2):391-420. PMID: 21184054. https://doi.org/10.1007/s00198-010-1501-1.
Reyes-García R, Rozas-Moreno P, López-Gallardo G, et al. Serum levels of bone resorption markers are decreased in patients with type 2 diabetes. Acta Diabetol. 2013;50(1):47-52. PMID: 22042129. https://doi.org/10.1007/s00592-011-0347-0.
Yamamoto M, Yamaguchi T, Nawata K, Yamauchi M, Sugimoto T. Decreased PTH levels accompanied by low bone formation are associated with vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. 2012;97(4):1277-84. PMID: 22337915. https://doi.org/10.1210/jc.2011-2537.
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. PMID: 22740707 PMCID: PMC3431571. https://doi.org/10.1210/jc.2012-1546.
Bhattoa HP, Wamwaki J, Kalina E, Foldesi R, Balogh A, Antal-Szalmas P. Serum sclerostin levels in healthy men over 50 years of age. J Bone Miner Metab. 2013;31(5):579-84. PMID: 23525828. https://doi.org/10.1007/s00774-013-0451-z.
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. PMID: 23845326. https://doi.org/10.1016/j.bone.2013.06.029.
Hamilton EJ, Rakic V, Davis WA, et al. A five-year prospective study of bone mineral density in men and women with diabetes: The Fremantle Diabetes Study. Acta Diabetol. 2012;49(2):153-8. PMID: 21971710. https://doi.org/10.1007/s00592-011-0324-7.
Akin O, Göl K, Aktürk M, Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol. 2003;17(1):19-29. PMID: 12724015.
Jiajue R, Jiang Y, Wang O, et al. Suppressed bone turnover was associated with increased osteoporotic fracture risks in non-obese postmenopausal Chinese women with type 2 diabetes mellitus. Osteoporos Int. 2014;25(8):1999-2005. PMID: 24760246. https://doi.org/10.1007/s00198-014-2714-5.
Bhattoa HP, Onyeka U, Kalina E, et al. Bone metabolism and the 10-year probability of hip fracture and a major osteoporotic fracture using the country-specific FRAX algorithm in men over 50 years of age with type 2 diabetes mellitus: A case-control study. Clin Rheumatol. 2013;32(8):1161-7. PMID: 23588883.https://doi.org/10.1007/s10067-013-2254-y.
Gaudio A, Privitera F, Battaglia K, et al. Sclerostin levels associated with inhibition of the Wnt/β-catenin signaling and reduced bone turnover in type 2 diabetes mellitus. J Clin Endocrinol Metab. 2012;97(10):3744-50. PMID: 22855334. https://doi.org/10.1210/jc.2012-1901.
Hernández JL, Olmos JM, Romaña G, et al. Bone turnover markers in statin users: A population-based analysis from the Camargo Cohort Study. Maturitas. 2013;75(1):67-73. PMID: 23489550. https://doi.org/ 10.1016/j.maturitas.2013.02.003.
Sarkar P, Choudhury A. 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. 2013;17(12):1631-5. PMID: 23832730.
Movahed A, Larijani B, Nabipour I, et al. 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. 2012;30(6):683-91. PMID: 22752126. https://doi.org/10.1007/s00774-012-0367-z.
Sosa M, Dominguez M, Navarro MC, et al. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications. 1996;10(4):201-5. PMID: 8835919.
Chen H, Li X, Yue R, Ren X, Zhang X, Ni A. The effects of diabetes mellitus and diabetic nephropathy on bone and mineral metabolism in T2DM patients. Diabetes Res Clin Pract. 2013;100(2):272-6. PMID: 23522918. https://doi.org/10.1016/j.diabres.2013.03.007.
Published
How to Cite
Issue
Section
License
Journal of the ASEAN Federation of Endocrine Societies is licensed under a Creative Commons Attribution-NonCommercial 4.0 International. (full license at this link: http://creativecommons.org/licenses/by-nc/3.0/legalcode).
To obtain permission to translate/reproduce or download articles or use images FOR COMMERCIAL REUSE/BUSINESS PURPOSES from the Journal of the ASEAN Federation of Endocrine Societies, kindly fill in the Permission Request for Use of Copyrighted Material and return as PDF file to jafes@asia.com or jafes.editor@gmail.com.
A written agreement shall be emailed to the requester should permission be granted.