Determinants of bone strength and quality in diabetes mellitus in humans

Bone

Volumn 82, Issue , 2016, Pages 28-34

  Farr, Joshua N ^a   Khosla, Sundeep ^a  

^a MAYO CLINIC   (United States)

Author keywords

Bone quality; Bone strength; Diabetes; HRpQCT

Indexed keywords

ADVANCED GLYCATION END PRODUCT; INSULIN; SCLEROSTIN;

BONE DENSITY; BONE FRAGILITY; BONE MINERAL; BONE QUALITY; BONE STRENGTH; BONE STRUCTURE; BONE TURNOVER; COMPUTER ASSISTED TOMOGRAPHY; CORTICAL BONE; DIABETIC PATIENT; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE DURATION; DUAL ENERGY X RAY ABSORPTIOMETRY; FRACTURE; GLYCEMIC CONTROL; HIGH RISK PATIENT; HUMAN; IN VIVO STUDY; MUSCULOSKELETAL SYSTEM PARAMETERS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSSIFICATION; OSTEOLYSIS; PATHOGENESIS; POROSITY; POSTMENOPAUSE; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; REVIEW; SCLEROSTIN BLOOD LEVEL; ANIMAL; BONE REMODELING; DIABETES MELLITUS; FRACTURES, BONE; METABOLISM; PHYSIOLOGY;

ANIMALS; BONE DENSITY; BONE REMODELING; DIABETES MELLITUS; FRACTURES, BONE; HUMANS;

EID: 84954371612     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.07.027     Document Type: Review

References (85)

1. Leslie W.D., Rubin M.R., Schwartz A.V., Kanis J.A. Type 2 diabetes and bone. J. Bone Miner. Res. 2012, 27:2231-2237.
2. Hamann C., Kirschner S., Gunther K.P., Hofbauer L.C. Bone, sweet bone-osteoporotic fractures in diabetes mellitus. Nat. Rev. Endocrinol. 2012, 8:297-305.
3. 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, 18:427-444.
4. Janghorbani M., Van Dam R.M., Willett W.C., Hu F.B. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am. J. Epidemiol. 2007, 166:495-505.
5. Hofbauer L., Brueck C.C., Singh S.K., Dobnig H. Osteoporosis in patients with diabetes mellitus. J. Bone Miner. Res. 2007, 22:1317-1328.
6. Strotmeyer E.S., Cauley J.A., Schwartz A.V., Nevitt M.C., Resnick H.E., Zmuda J.M., Bauer D.C., Tylavsky F.A., de Rekeneire N., Harris T.B., Newman A.B. 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, 19:1084-1091.
7. Schwartz A.V., Sellmeyer D.E., Ensrud K.E., Cauley J.A., Tabor H.K., Schreiner P.J., Jamal S.A., Black D.M., Cummings S.R. Older women with diabetes have an increased risk of fracture: a prospective study. J. Clin. Endocrinol. Metab. 2001, 86:32-38.
8. Bonds D.E., Larson J.C., Schwartz A.V., Strotmeyer E.S., Robbins J., Rodriguez B.L., Johnson K.C., Margolis K.L. Risk of fracture in women with type 2 diabetes: the Women's Health Initiative Observational Study. J. Clin. Endocrinol. Metab. 2006, 91:3404-3410.
9. Schwartz A.V., Vittinghoff E., Bauer D.C., Hillier T.A., Strotmeyer E.S., Ensrud K.E., Donaldson M.G., Cauley J.A., Harris T.B., Koster A., Womack C.R., Palermo L., Black D.M. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 2011, 305:2184-2192.
10. Giangregorio L.M., Leslie W.D., Lix L.M., Johansson H., Oden A., McCloskey E., Kanis J.A. FRAX underestimates fracture risk in patients with diabetes. J. Bone Miner. Res. 2012, 27:301-308.
11. Dawson-Hughes B., Lindsay R., Khosla S., Melton L.J., Tosteson A.N.A., Favus M.J., Baim S. Clinician's guide to prevention and treatment of osteoporosis 2008, National Osteoporosis Foundation, Washington, D.C.
12. Fulzele K., Riddle R.C., DiGirolamo D.J., Cao X., Wan C., Chen D., Faugere M.-C., Aja S., Hussain M.A., Bruning J.C., Clemens T.L. Insulin receptor signaling in osteoblasts regulates postnatal bone acquistition and body composition. Cell 2010, 142:309-319.
13. Krakauer J.C., McKenna M.J., Buderer N.F., Rao D.S., F.W.W, Parfitt A.M. Bone loss and bone turnover in diabetes. Diabetes 1995, 44:775-782.
14. Shanbhogue V.V., Hansen S., Frost M., Jorgensen N.R., Hermann A.P., Henriksen J.E., Brixen K. Bone geometry, volumetric density, microarchitecture and estimated bone strength assessed by HRpQCT in adult patients with type I diabetes mellitus. J. Bone Miner. Res. 2015, 10.1002/jbmr.2573.
15. Schwartz A.V., Vittinghoff E., Sellmeyer D.E., Feingold K.R., De Rekeneire N., Strotmeyer E.S., Shorr R.I., Vinik A.I., Odden M.C., Park S.W., Faulkner K.A., Harris T.B. Diabetes-related complications, glycemic control, and falls in older adults. Diabetes Care 2008, 31:391-396.
16. Schwartz A.V., Hillier T.A., Sellmeyer D.E., Resnick H.E., Gregg E., Ensrud K.E., Schreiner P.J., Margolis K.L., Cauley J.A., Nevitt M.C., Black D.M., Cummings S.R. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care 2002, 25:1749-1754.
17. Loke Y.K., Singh S., Furberg C.D. Long-term use of thiazolidinediones and fractures in type 2 diabetes: a meta-analysis. CMAJ 2009, 180:32-39.
18. Melton L.J., Leibson C.L., Achenbach S.J., Therneau T.M., Khosla S. Fracture risk in type 2 diabetes: update of a population-based study. J. Bone Miner. Res. 2008, 23:1334-1342.
19. Cortizo A.M., Sedlinsky C., McCarthy A.D., Blanco A., Schurman L. Osteogenic actions of the anti-diabetic drug metformin on osteoblasts in culture. Eur. J. Pharmacol. 2006, 536:38-46.
20. Oei L., Zillikens M.C., Dehghan A., Buitendijk G.H., Castano-Betancourt M.C., Estrada K., Stolk L., Oei E.H., van Meurs J.B., Janssen J.A., Hofman A., van Leeuwen J.P., Witteman J.C., Pols H.A., Uitterlinden A.G., Klaver C.C., Franco O.H., Rivadeneira F. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam study. Diabetes Care 2013, 36:1619-1628.
21. Schwartz A.V., Margolis K.L., Sellmeyer D.E., Vittinghoff E., Ambrosius W.T., Bonds D.E., Josse R.G., Schnall A.M., Simmons D.L., Hue T.F., Palermo L., Hamilton B.P., Green J.B., Atkinson H.H., O'Connor P.J., Force R.W., Bauer D.C. Intensive glycemic control is not associated with fractures or falls in the ACCORD randomized trial. Diabetes Care 2012, 35:1525-1531.
22. Oei L., Zillikens M.C., Dehghan A., Buitendijk G.H., Castano-Betancourt M.C., Estrada K., Stolk L., Oei E.H.G., Van Meurs J.B., Janssen J.A., Hofman A., van Leeuwen J.P.T.M., Witteman J.C., Pols H.A., Uitterlinden A.G., Klaver C.C., Franco O.H., Rivadeneira F. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control. Diabetes Care 2013, 36:1619-1628.
23. 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.
24. Keegan T.H., Schwartz A.V., Bauer D.C., Sellmeyer D.E., Kelsey J.L. 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, 27:1547-1553.
25. Schwartz A.V., Sellmeyer D.E., Strotmeyer E.S., Tylavsky F.A., Feingold K.R., Resnick H.E., Shorr R.I., Nevitt M.C., Black D.M., Cauley J.A., Cummings S.R., Harris T.B. Diabetes and bone loss at the hip in older black and white adults. J. Bone Miner. Res. 2005, 20:596-603.
26. Schwartz A.V., Ewing S.K., Porzig A.M., McCulloch C.E., Resnick H.E., Hillier T.A., Ensrud K.E., Black D.M., Nevitt M.C., Cummings S.R., Sellmeyer D.E. Diabetes and change in bone mineral density at the hip, calcaneus, spine, and radius in older women. Front. Endocrinol. (Lausanne) 2013, 4:62. 10.3389/fendo.2013.00062. eCollection 2013.
27. Hillier T.A., Stone K.L., Bauer D.C., Rizzo J.H., Pedula K.L., Cauley J.A., Ensrud K.E., Hochberg M.C., Cummings S.R. 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, 167:155-160.
28. Cawthon P.M., Ewing S.K., Mackey D.C., Fink H.A., Cummings S.R., Ensrud K.E., Stefanick M.L., Bauer D.C., Cauley J.A., Orwoll E.S. Change in hip bone mineral density and risk of subsequent fractures in older men. J. Bone Miner. Res. 2012, 27:2179-2188.
29. Nelson H.D., Helfand M., Woolf S.H., Allan J.D. Screening for postmenopausal osteoporosis: a review of the evidence for the U.S. Preventive Services Task Force. Ann. Intern. Med. 2002, 137:529-541.
30. Harvey N.C., Gluer C.C., Binkley N.C., McCloskey E.V., Brandi M.L., Cooper C., Kendler D., Lamy O., Laslop A., Camargos B.M., Reginster J.Y., Rizzoli R., Kanis J.A. Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 2015, 78:216-224.
31. Leslie W.D., Aubry-Rozier B., Lamy O., Hans D. TBS (trabecular bone score) and diabetes-related fracture risk. J. Clin. Endocrinol. Metab. 2013, 98:602-609.
32. Dhaliwal R., Cibula D., Ghosh C., Weinstock R.S. Bone quality assessment in type 2 diabetes mellitus. Osteoporos. Int. 2014, 25:1969-1973.
33. Kim J.H., Choi H.J., Ku E.J., Kim K.M., Kim S.W., Cho N.H., Shin C.S. Trabecular bone score as an indicator for skeletal deterioration in diabetes. J. Clin. Endocrinol. Metab. 2015, 100:475-482.
34. Melton L.J., Riggs B.L., Leibson C.L., Achenbach S.J., Camp J.J., Bouxsein M.L., Atkinson E.J., Robb R.A., Khosla S. A bone structural basis for fracture risk in diabetes. J. Clin. Endocrinol. Metab. 2008, 93:4804-4809.
35. Petit M.A., Paudel M.L., Taylor B.C., Hughes J.M., Strotmeyer E.S., Schwartz A.V., Cauley J.A., Zmuda J.M., Hoffman A.R., Ensrud K.E. Bone mass and strength in older men with type 2 diabetes: the Osteoporotic Fractures in Men Study. J. Bone Miner. Res. 2010, 25:285-291.
36. Seeman E., Delmas P.D. Bone quality - the material and structural basis of bone strength and fragility. N. Engl. J. Med. 2006, 354:2250-2261.
37. Chavassieux P., Seeman E., Delmas P.D. Insights into material and structural basis of bone fragility from diseases associated with fractures: how determinants of the biomechanical properties of bone are compromised by disease. Endocr. Rev. 2007, 28:151-164.
38. Burghardt A.J., Issever A.S., Schwartz A.V., Davis K.A., Masharani U., Majumdar S., Ling T.M. 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, 95:5045-5055.
39. Shu A., Yin M.T., Stein E., Cremers S., Dworakowski E., Ives R., Rubin M.R. Bone structure and turnover in type 2 diabetes mellitus. Osteoporos. Int. 2012, 23:635-641.
40. Farr J.N., Drake M.T., Amin S., Melton L.J., McCready L.K., Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J. Bone Miner. Res. 2014, 29:787-795.
41. Patsch J.M., Burghardt A.J., Yap S.P., Baum T., Schwartz A.V., Joseph G.B., Link T.M. Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J. Bone Miner. Metab. 2013, 28:313-324.
42. Liu X.S., Cohen A., Shane E., Yin P.T., Stein E.M., Rogers H., Kokolus S.L., McMahon D.J., Lappe J.M., Recker R.R., Lang T., Guo X.E. Bone density, geometry, microstructure, and stiffness: relationships between peripheral and central skeletal sites assessed by DXA, HRpQCT, and cQCT in premenopausal women. J. Bone Miner. Res. 2010, 25:2229-2238.
43. Yu E.W., Putman M.S., Derrico N., Abrishamanian-Garcia G., Finkelstein J.S., Bouxsein M.L. Defects in cortical microarchitecture among African-American women with type 2 diabetes. Osteoporos. Int. 2015, 26:673-679.
44. Hansma P.K., Turner P.J., Fanter G.E. Bone diagnostic instrument. Rev. Sci. Instrum. 2006, 77:075105.
45. Hansma P., Turner P., Drake B., Yurtsev E., Proctor A., Mathews P., Lelujian J., Randall C., Adams J., Jungmann R., Garza-de-Leon F., Fantner G., Mkrtchyan H., Pontin M., Weaver A., Brown M.B., Sahar N., Rossello R., Kohn D. The bone diagnostic instrument II: indentation distance increase. Rev. Sci. Instrum. 2008, 79:064303.
46. Randall C., Mathews P., Yurtsev E., Sahar N., Kohn D., Hansma P. The bone diagnostic instrument III: testing mouse femora. Rev. Sci. Instrum. 2009, 80:065108.
47. Hansma P., Yu H., Schultz D., Rodriguez A., Yurtsev E.A., Orr J., Tang S., Miller J., Wallace J., Zok F., Li C., Souza R., Proctor A., Brimer D., Nogues-Solan X., Mellbovsky L., Pena M.J., Diez-Ferrer O., Mathews P., Randall C., Kuo A., Chen C., Peters M., Kohn D., Buckley J., Li X., Pruitt L., Diez-Perez A., Alliston T., Weaver V., Lotz J. The tissue diagnostic instrument. Rev. Sci. Instrum. 2009, 80:054303.
48. Bridges D., Randall C., Hansma P.K. A new device for performing reference point indentation without a reference probe. Rev. Sci. Instrum. 2012, 83:044301.
49. Diez-Perez A., Guerri R., Nogues X., Caceres E., Pena M.J., Mellibovsky L., Randall C., Bridges D., Weaver J.C., Proctor A., Brimer D., Koester K.J., Ritchie R.O., Hansma P.K. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J. Bone Miner. Res. 2010, 25:1877-1885.
50. Guerri-Fernandez R.C., Nogues X., Quesada Gomex J.M., Torres del Pliego E., Puig L., Garcia-Giralt N., Yoskovitz G., Mellibovsky L., Hansma P.K., Diez-Perez A. Microindentation for in vivo measurement of bone tissue material properties in atypical femoral fracture patients and controls. J. Bone Miner. Res. 2013, 28:162-168.
51. Randall C., Bridges D., Guerri R., Nogues X., Puig L., Torres E., Mellibovsky L., Hoffseth K., Stalbaum T., Srikanth A., Weaver J.C., Rosen S., Barnard H., Brimer D., Proctor A., Candy A., Saldana C., Chandrasekar S., Lescun T., Nielson C.M., Orwoll E., Herthel D., Kopeikin H., Yang H.T., Farr J.N., McCready L., Khosla S., Diez-Perez A., Hansma P.K. Applications of a new handheld reference point indentation instrument measuring bone material strength. J. Med. Device 2013, 7:410051-410056.
52. Jepsen K.J., Schlecht S.H. Biomechanical mechanisms: resolving the apparent conundrum of why individuals with type II diabetes show increased fracture incidence despite having normal BMD. J. Bone Miner. Res. 2014, 29:784-786.
53. Sroga G.E., Vashishth D. Effects of bone matrix proteins on fracture and fragility in osteoporosis. Curr. Osteoporos. Rep. 2012, 10:141-150.
54. Ahmed N., Thornalley P.J. Quantitative screening of protein biomarkers of early glycation, advanced glycation, oxidation and nitrosation in cellular and extracellular proteins by tandem mass spectrometry multiple reaction monitoring. Biochem. Soc. Trans. 2003, 31:1417-1422.
55. Garnero P., Borel O., Gineyts E., Duboeuf F., Solberg H., Bouxsein M.L., Christiansen C., Delmas P.D. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone 2006, 38:300-309.
56. Karim L., Vashishth D. Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS ONE 2012, 7:e35047.
57. Karim L., Tang S.Y., Sroga G.E., Vashishth D. Differences in non-enzymatic glycation and collagen cross-links between human cortical and cancellous bone. Osteoporos. Int. 2013, 24:2441-2447.
58. McCarthy A.D., Uemura T., Etcheverry S.B., Cortizo A.M. Advanced glycation endproducts interfere with integrin-mediated osteoblastic attachment to a type-I collagen matrix. Int. J. Biochem. Cell Biol. 2004, 36:840-848.
59. Kume S., Kato S., Si Yamagishi, Inagaki Y., Ueda S., Arima N., Okawa T., Kojiro M., Nagata K. Advanced glycation end-products attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone. J. Bone Miner. Res. 2005, 20:1647-1658.
60. Sanguineti R., Storace D., Monacelli F., Federici A., Odetti P. Pentosidine effects on human osteoblasts in vitro. Ann. N. Y. Acad. Sci. 2008, 1126:166-172.
61. Sroga G.E., Vashishth D. UPLC methodology for identification and quantification of naturally fluorescent crosslinks in proteins: a study of bone collagen. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2011, 879:379-385.
62. 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, 93:1013-1019.
63. Schwartz A.V., Garnero P., Hillier T.A., Sellmeyer D.E., Strotmeyer E.S., Feingold K.R., Resnick H.E., Tylavsky F.A., Black D.M., Cummings S.R., Harris T.B., Bauer D.C. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J. Clin. Endocrinol. Metab. 2009, 94:2380-2386.
64. Reddy S., Bichler J., Wells-Knecht K.J., Thorpe S.R., Baynes J.W. N epsilon-(carboxymethyl)lysine is a dominant advanced glycation end product (AGE) antigen in tissue proteins. Biochemistry 1995, 34:10872-10878.
65. Hein G., Wiegand R., Lehmann G., Stein G., Franke S. Advanced glycation end-products pentosidine and N epsilon-carboxymethyllysine are elevated in serum of patients with osteoporosis. Rheumatology 2003, 42:1242-1246.
66. Barzilay J., Buzkova P., Zieman S.J., Kizer J.R., Djousse L., Ix J.H., Tracy R.P., Siscovick D.S., Cauley J.A., Mukamal K.J. Circulating levels of carboxy-methyl-lysine (CML) are associated with hip fracture risk: The Cardiovascular Health Study. J. Bone Miner. Res. 2014, 29:1061-1066.
67. Dorrian C.A., Cathcart S., Clausen J., Shapiro D., Dominiczak M.H. Factors in human serum interfere with the measurement of advanced glycation endproducts. Cell. Mol. Biol. 1998, 44:1069-1079.
68. Manavalan J.S., Cremers S., Dempster D.W., Zhou H., Dworakowski E., Kode A., Kousteni S., Rubin M.R. Circulating osteogenic precursor cells in type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2012, 97:3240-3250.
69. Okazaki R., Totsuka Y., Hamano K., Ajima M., Miura M., Hirota Y., Hata K., Fukumoto S., Matsumoto T. Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J. Clin. Endocrinol. Metab. 1997, 82:2915-2920.
70. Gerdhem P., Isaksson A., Akesson K., Obrant K.J. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos. Int. 2005, 16:1506-1512.
71. Dobnig H., Piswanger-Solkner J.C., Roth M., Obermayer-Pietsch B., Tiran A., Strele A., Maier E., Maritschnegg P., Sieberer C., Fahrleitner-Pammer A. Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J. Clin. Endocrinol. Metab. 2006, 91:3355-3363.
72. Oz S.G., Guven G.S., Kilicarslan A., Calik N., Beyazit Y., Sozen T. Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus. J. Natl. Med. Assoc. 2006, 98:1598-1604.
73. Kanazawa I., Yamaguchi T., Yamamoto M., Yamauchi M., Kurioka S., Yano S., Sugimoto T. Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2009, 94:45-49.
74. 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, 97:1277-1284.
75. Garcia-Martin A., Rozas-Moreno P., Reyes-Garcia R., Morales-Santana S., Garcia-Fontana B., Garcia-Salcedo J.A., Munoz-Torres M. Circulating levels of sclerostin are increased in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 2012, 97:234-241.
76. Gennari L., Merlotti D., Valenti R., Ceccarelli E., Ruvio M., Pietrini M.G., Capodarca C., Franci M.B., Campagna M.S., Calabro A., Cataldo D., Stolakis K., Dotta F., Nuti R. Circulating sclerostin levels and bone turnover in type 1 and type 2 diabetes. J. Clin. Endocrinol. Metab. 2012, 97:1737-1744.
77. Gaudio A., Privitera F., Battaglia K., Torrisi V., Sidoti M.H., Pulvirenti I., Canzonieri E., Tringali G., Fiore C.E. 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, 97:3744-3750.
78. Khosla S., Westendorf J.J., Oursler M.J. Building bone to reverse osteoporosis and repair fractures. J. Clin. Invest. 2008, 118:421-428.
79. Tang S.Y., Allen M.R., Phipps R., Burr D.B., Vashishth D. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos. Int. 2009, 20:887-894.
80. Allen M.R., Burr D.B. Bisphosphonate effects on bone turnover, microdamage, and mechanical properties: what we think we know and what we know that we don't know. Bone 2011, 49:56-65.
81. Meier C., Schwartz A.V., Egger A., Lecka-Czernik B. Effects of diabetes drugs on the skeleton. Bone 2015, (Epub ahead of print). 10.1016/j.bone.2015.04.026.
82. Gilbert M.P., Pratley R.E. The impact of diabetes treatments on bone health in patients with type 2 diabetes mellitus. Endocr. Rev. 2015, (Epub 2015 Mar 4). 10.1210/er.2012-1042.
83. Saito M., Fujii K., Mori Y., Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos. Int. 2006, 17:1514-1523.
84. Khosravi R., Sodek K.L., Faibish M., Trackman P.C. Collagen advanced glycation inhibits its Discoidin Domain Receptor 2 (DDR2)-mediated induction of lysyl oxidase in osteoblasts. Bone 2014, 58:33-41.
85. Ke H.Z., Richards W.G., Li X., Ominsky M.S. Sclerostin and dickkopf-1 as therapeutic targets in bone diseases. Endocr. Rev. 2012, 33:747-783.