Osteoporosis among patients with type 1 and type 2 diabetes

Diabetes and Metabolism

Volumn 34, Issue 3, 2008, Pages 193-205

  Rakel A ^a,b   Sheehy, O ^a   Rahme, E ^b   LeLorier, J ^a  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Bone mineral density; Diabetes mellitus type 1 and type 2; Fractures; Osteopenia; Osteoporosis; Review

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CALCIUM; COLECALCIFEROL; DARGLITAZONE; GLIBENCLAMIDE; INSULIN; LEPTIN; METFORMIN; NETOGLITAZONE; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; SOMATOMEDIN C;

BONE ATROPHY; BONE DENSITY; BONE METABOLISM; BONE STRUCTURE; BONE TURNOVER; CALCIUM INTAKE; CORTICOSTEROID INDUCED OSTEOPOROSIS; DIABETIC MICROANGIOPATHY; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC PATIENT; DIABETIC RETINOPATHY; DISEASE ASSOCIATION; EVIDENCE BASED PRACTICE; EXERCISE; FRAGILITY FRACTURE; GLYCEMIC CONTROL; HUMAN; HYPOGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN METABOLISM; MORPHOMETRICS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSSIFICATION; OSTEOPOROSIS; PATIENT ASSESSMENT; POSTMENOPAUSE OSTEOPOROSIS; REVIEW; RISK ASSESSMENT; RISK FACTOR; VITAMIN SUPPLEMENTATION;

ADULT; BONE DENSITY; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FRACTURES, BONE; HUMANS; OSTEOPOROSIS; PREVALENCE;

EID: 44849133629     PISSN: 12623636     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.diabet.2007.10.008     Document Type: Review

References (122)

1. Albright F., and Reifenstein E.C. Bone development in diabetic children: a roentgen study. Am J Med Sci 174 (1948) 313-319
2. Christensen J.O., and Svendsen O.L. Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int 10 (1999) 307-311
3. Gunczler P., Lanes R., Paoli M., Martinis R., Villaroel O., and Weisinger J.R. Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14 (2001) 525-528
4. Hampson G., Evans C., Petitt R.J., Evans W.D., Woodhead S.J., Peters J.R., et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia 41 (1998) 1314-1320
5. Kao W.H., Kammerer C.M., Schneider J.L., Bauer R.L., and Mitchell B.D. Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res 34 (2003) 399-406
6. Kayath M.J., Dib S.A., and Vieira J.G. Prevalence and magnitude of osteopenia associated with insulin-dependent diabetes mellitus. J Diabetes Complications 8 (1994) 97-104
7. Krakauer J.C., McKenna M.J., Buderer N.F., Rao D.S., Whitehouse F.W., and Parfitt A.M. Bone loss and bone turnover in diabetes. Diabetes 44 (1995) 775-782
8. Miazgowski T., and 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 8 (1998) 399-403
9. Strotmeyer E.S., Cauley J.A., Schwartz A.V., Nevitt M.C., Resnick H.E., Zmuda J.M., 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 19 (2004) 1084-1091
10. van Daele P.L.A., Stolk R.P., Burger H., Algra D., Grobbee D.E., Hofman A., et al. Bone Density in Non-Insulin-Dependent Diabetes Mellitus: The Rotterdam Study. Ann Intern Med 122 (1995) 409-414
11. Leidig-Bruckner G., and Ziegler R. Diabetes mellitus a risk for osteoporosis?. Exp Clin Endocrinol Diabetes 109 Suppl. 2 (2001) S493-S514
12. Schwartz A.V. Diabetes mellitus: does it affect bone?. Calcif Tissue Int 73 (2003) 515-519
13. Thrailkill K.M., Lumpkin Jr. C.K., Bunn R.C., Kemp S.F., and Fowlkes J.L. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289 (2005) E735-E745
14. McNair P., Madsbad S., Christiansen C., Faber O.K., Transbol I., and Binder C. Osteopenia in insulin treated diabetes mellitus. Its relation to age at onset, sex and duration of disease. Diabetologia 15 (1978) 87-90
15. Rosenbloom A.L., Lezotte D.C., Weber F.T., Gudat J., Heller D.R., Weber M.L., et al. Diminution of bone mass in childhood diabetes. Diabetes 26 (1977) 1052-1055
16. Santiago J.V., McAlister W.H., Ratzan S.K., Bussman Y., Haymond M.W., Shackelford G., et al. Decreased cortical thickness & osteopenia in children with diabetes mellitus. J Clin Endocrinol Metab 45 (1977) 845-848
17. Campos Pastor M.M., Lopez-Ibarra P.J., Escobar-Jimenez F., Serrano Pardo M.D., and Garcia-Cervigon A.G. Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int 11 (2000) 455-459
18. De Schepper J., Smitz J., Rosseneu S., Bollen P., and Louis O. Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 50 (1998) 193-196
19. Forst T., Pfutzner A., Kann P., Schehler B., Lobmann R., Schafer H., et al. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 12 (1995) 874-879
20. Gunczler P., Lanes R., Paz-Martinez V., Martins R., Esaa S., Colmenares V., et al. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab 11 (1998) 413-419
21. Kayath M.J., Tavares E.F., Dib S.A., and Vieira J.G.H. Prospective bone mineral density evaluation in patients with insulin-dependent diabetes mellitus. J Diabetes Complications 12 (1998) 133
22. Lunt H., Florkowski C.M., Cundy T., Kendall D., Brown L.J., Elliot J.R., et al. A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes Res Clin Pract 40 (1998) 31-38
23. Munoz-Torres M., Jodar E., Escobar-Jimenez F., Lopez-Ibarra P.J., and Luna J.D. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int 58 (1996) 316-319
24. Rozadilla A., Nolla J.M., Montana E., Fiter J., Gomez-Vaquero C., Soler J., et al. Bone mineral density in patients with type 1 diabetes mellitus. Joint Bone Spine 67 (2000) 215-218
25. Kemink S.A., Hermus A.R., Swinkels L.M., Lutterman J.A., and Smals A.G. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23 (2000) 295-303
26. Lopez-Ibarra P.J., Pastor M.M., Escobar-Jimenez F., Pardo M.D., Gonzalez A.G., Luna J.D., et al. Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract 7 (2001) 346-351
27. Tuominen J.T., Impivaara O., Puukka P., and Ronnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22 (1999) 1196-1200
28. Ersoy B., Goksen D., Darcan S., Mavi E., and Ozturk C. Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66 (1999) 375-379
29. Lettgen B., Hauffa B., Mohlmann C., Jeken C., and 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 43 (1995) 173-175
30. Heap J., Murray M.A., Miller S.C., Jalili T., and Moyer-Mileur L.J. Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr 144 (2004) 56
31. Liu E.Y., Wactawski-Wende J., Donahue R.P., Dmochowski J., Hovey K.M., and Quattrin T. Does low bone mineral density start in post-teenage years in women with type 1 diabetes?. Diabetes Care 26 (2003) 2365-2369
32. Valerio G., del Puente A., Esposito-del Puente A., Buono P., Mozzillo E., and Franzese A. The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 58 (2002) 266-272
33. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes-a meta-analysis. Osteoporos Int 18 (2007) 427-444
34. Barrett-Connor E., and Holbrook T.L. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. Jama 268 (1992) 3333-3337
35. de Liefde I., van der Klift M., de Laet C.E., van Daele P.L., Hofman A., and Pols H.A. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16 (2005) 1713-1720
36. Dennison E.M., Syddall H.E., Aihie Sayer A., Craighead S., Phillips D.I., and 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 47 (2004) 1963-1968
37. el Miedany Y.M., el Gaafary S., and el Baddini M.A. Osteoporosis in older adults with non-insulin-dependent diabetes mellitus: is it sex related?. Clin Exp Rheumatol 17 (1999) 561-567
38. Isaia G.C., Ardissone P., Di Stefano M., Ferrari D., Martina V., Porta M., et al. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 36 (1999) 35-38
39. Kwon D.J., Kim J.H., Chung K.W., Kim J.H., Lee J.W., Kim S.P., 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 22 (1996) 157-162
40. Lunt H., Florkowski C.M., Cook H.B., and Whitehead M.R. Bone mineral density, type 1 diabetes, and celiac disease. Diabetes Care 24 (2001) 791-792
41. Rishaug U., Birkeland K.I., Falch J.A., and Vaaler S. Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest 55 (1995) 257-262
42. Sahin G., Bagis S., Cimen O.B., Ozisik S., Guler H., and Erdogan C. Lumbar and femoral bone mineral density in type 2 Turkish diabetic patients. Acta Medica (Hradec Kralove) 44 (2001) 141-143
43. Sert M., Tetiker T., Kirim S., Soyupak S., Canataroglu A., and Kocak M. Type 2 diabetes mellitus and osteopenia: is there an association?. Acta Diabetol 40 (2003) 105-108
44. Sosa M., Dominguez M., Navarro M.C., Segarra M.C., Hernandez D., de Pablos P., et al. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10 (1996) 201-205
45. Bridges M.J., Moochhala S.H., Barbour J., and Kelly C.A. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol 42 (2005) 82-86
46. Majima T., Komatsu Y., Yamada T., Koike Y., Shigemoto M., Takagi C., et al. Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int 16 (2005) 907-913
47. Al-Maatouq M.A., El-Desouki M.I., Othman S.A., Mattar E.H., Babay Z.A., and Addar M. Prevalence of osteoporosis among postmenopausal females with diabetes mellitus. Saudi Med J 25 (2004) 1423-1427
48. Resnick D., Shaul S.R., and Robins J.M. Diffuse idiopathic skeletal hyperostosis (DISH): Forestier's disease with extraspinal manifestations. Radiology 115 (1975) 513-524
49. The Study of Osteoporotic Fractures Research Group, Kelsey J.L., Browner W.S., Seeley D.G., Nevitt M.C., and Cummings S.R. Risk factors for fractures of the distal forearm and proximal humerus. Am J Epidemiol 135 (1992) 477-489
50. Forsen L., Meyer H.E., Midthjell K., and Edna T.H. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42 (1999) 920-925
51. Nicodemus K.K., and Folsom A.R. Type 1 and Type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24 (2001) 1192-1197
52. Miao J., Brismar K., Nyren O., Ugarph-Morawski A., and Ye W. Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care 28 (2005) 2850-2855
53. Janghorbani M., Feskanich D., Willett W.C., and Hu F. Prospective study of diabetes and risk of hip fracture: The Nurses' Health Study. Diabetes Care 29 (2006) 1573-1578
54. Vestergaard P., Rejnmark L., and Mosekilde L. Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48 (2005) 1292-1299
55. Schwartz A.V., Sellmeyer D.E., Ensrud K.E., Cauley J.A., Tabor H.K., Schreiner P.J., et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86 (2001) 32-38
56. Ottenbacher K.J., Ostir G.V., Peek M.K., Goodwin J.S., and Markides K.S. Diabetes mellitus as a risk factor for hip fracture in Mexican American older adults. J Gerontol A Biol Sci Med Sci 57 (2002) M648-M653
57. Taylor B.C., Schreiner P.J., Stone K.L., Fink H.A., Cummings S.R., Nevitt M.C., et al. Long-term prediction of incident hip fracture risk in elderly white women: study of osteoporotic fractures. J Am Geriatr Soc 52 (2004) 1479-1486
58. Dobnig H., Piswanger-Solkner J.C., 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 91 (2006) 3355-3363
59. Strotmeyer E.S., Cauley J.A., Schwartz A.V., Nevitt M.C., Resnick H.E., Bauer D.C., 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 165 (2005) 1612-1617
60. Bonds D.E., Larson J.C., Schwartz A.V., Strotmeyer E.S., Robbins J., Rodriguez B.L., et al. Risk of fracture in women with type 2 diabetes: the Women's Health Initiative Observational Study. J Clin Endocrinol Metab 91 (2006) 3404-3410
61. Moyer-Mileur L.J., Dixon S.B., Quick J.L., Askew E.W., and Murray M.A. Bone mineral acquisition in adolescents with type 1 diabetes. The Journal of Pediatrics 145 (2004) 662
62. Wientroub S., Eisenberg D., Tardiman R., Weissman S.L., and Salama R. Is diabetic osteoporosis due to microangiopathy?. Lancet 2 (1980) 983
63. Vogt M.T., Cauley J.A., Kuller L.H., and Nevitt M.C. Bone mineral density and blood flow to the lower extremities: the study of osteoporotic fractures. J Bone Miner Res 12 (1997) 283-289
64. Clausen P., Feldt-Rasmussen B., Jacobsen P., Rossing K., Parving H.H., Nielsen P.K., et al. Microalbuminuria as an early indicator of osteopenia in male insulin-dependent diabetic patients. Diabet Med 14 (1997) 1038-1043
65. Rigalleau V., Lasseur C., Raffaitin C., Perlemoine C., Barthe N., Chauveau P., et al. Bone loss in diabetic patients with chronic kidney disease. Diabet Med 24 (2007) 91-93
66. Selby P.L., Shearing P.A., and Marshall S.M. Hydroxyproline excretion is increased in diabetes mellitus and related to the presence of microalbuminuria. Diabet Med 12 (1995) 240-243
67. Elder G.J., and Mackun K. 25-Hydroxyvitamin D deficiency and diabetes predict reduced BMD in patients with chronic kidney disease. J Bone Miner Res 21 (2006) 1778-1784
68. Pei Y., Hercz G., Greenwood C., Segre G., Manuel A., Saiphoo C., et al. Renal osteodystrophy in diabetic patients. Kidney Int 44 (1993) 159-164
69. Yamaguchi T., Kanno E., Tsubota J., Shiomi T., Nakai M., and Hattori S. Retrospective study on the usefulness of radius and lumbar bone density in the separation of hemodialysis patients with fractures from those without fractures. Bone 19 (1996) 549-555
70. Rix M., Andreassen H., and Eskildsen P. Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22 (1999) 827-831
71. Raskin P., Stevenson M.R., Barilla D.E., and Pak C.Y. The hypercalciuria of diabetes mellitus: its amelioration with insulin. Clin Endocrinol (Oxf) 9 (1978) 329-335
72. Thalassinos N.C., Hadjiyanni P., Tzanela M., Alevizaki C., and Philokiprou D. Calcium metabolism in diabetes mellitus: effect of improved blood glucose control. Diabet Med 10 (1993) 341-344
73. McNair P., Christensen M.S., Madsbad S., Christiansen C., and Transbol I. Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 96 (1981) 81-86
74. Heath Jr. H., Lambert P.W., Service F.J., and Arnaud S.B. Calcium homeostasis in diabetes mellitus. J Clin Endocrinol Metab 49 (1979) 462-466
75. Bertelloni S. The parathyroid hormone - 1,25-dihydroxyvitamin D endocrine system and magnesium status in insulin-dependent diabetes mellitus: current concepts. Magnes Res 5 (1992) 45-51
76. Thrailkill K.M., Liu L., Wahl E.C., Bunn R.C., Perrien D.S., Cockrell G.E., et al. Bone formation is impaired in a model of type 1 diabetes. Diabetes 54 (2005) 2875-2881
77. Raisz L.G. Local and systemic factors in the pathogenesis of osteoporosis. N Engl J Med 318 (1988) 818-828
78. Jehle P.M., Jehle D.R., Mohan S., and Bohm B.O. 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 159 (1998) 297-306
79. Thomas T. The complex effects of leptin on bone metabolism through multiple pathways. Curr Opin Pharmacol 4 (2004) 295
80. Thomas T., and Burguera B. Is leptin the link between fat and bone mass?. J Bone Miner Res 17 (2002) 1563-1569
81. Alexopoulou O., Jamart J., Devogelaer J.P., Brichard S., de Nayer P., and Buysschaert M. Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabetes Metab 32 (2006) 453-458
82. Burguera B., Hofbauer L.C., Thomas T., Gori F., Evans G.L., Khosla S., et al. Leptin reduces ovariectomy-induced bone loss in rats. Endocrinology 142 (2001) 3546-3553
83. Meunier P., Aaron J., Edouard C., and Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80 (1971) 147-154
84. Rozman C., Feliu E., Berga L., Reverter J.C., Climent C., and Ferran M.J. Age-related variations of fat tissue fraction in normal human bone marrow depend both on size and number of adipocytes: a stereological study. Exp Hematol 17 (1989) 34-37
85. Karsenty G. Minireview: transcriptional control of osteoblast differentiation. Endocrinology 142 (2001) 2731-2733
86. Lecka-Czernik B., Moerman E.J., Grant D.F., Lehmann J.M., Manolagas S.C., and Jilka R.L. Divergent effects of selective peroxisome proliferator-activated receptor-gamma 2 ligands on adipocyte versus osteoblast differentiation. Endocrinology 143 (2002) 2376-2384
87. Akune T., Ohba S., Kamekura S., Yamaguchi M., Chung U.I., Kubota N., et al. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 113 (2004) 846-855
88. Botolin S., Faugere M.C., Malluche H., Orth M., Meyer R., and McCabe L.R. Increased bone adiposity and peroxisomal proliferator-activated receptor-gamma2 expression in type I diabetic mice. Endocrinology 146 (2005) 3622-3631
89. Lecka-Czernik B., Gubrij I., Moerman E.J., Kajkenova O., Lipschitz D.A., Manolagas S.C., et al. Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARgamma2. J Cell Biochem 74 (1999) 357-371
90. Ali A.A., Weinstein R.S., Stewart S.A., Parfitt A.M., Manolagas S.C., and Jilka R.L. Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology 146 (2005) 1226-1235
91. Rzonca S.O., Suva L.J., Gaddy D., Montague D.C., and Lecka-Czernik B. Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology 145 (2004) 401-406
92. Sottile V., Seuwen K., and Kneissel M. Enhanced marrow adipogenesis and bone resorption in estrogen-deprived rats treated with the PPARgamma agonist BRL49653 (rosiglitazone). Calcif Tissue Int 75 (2004) 329-337
93. Lazarenko O.P., Rzonca S.O., Suva L.J., and Lecka-Czernik B. Netoglitazone is a PPAR-gamma ligand with selective effects on bone and fat. Bone 38 (2006) 74-84
94. Li M., Pan L.C., Simmons H.A., Li Y., Healy D.R., Robinson B.S., et al. Surface-specific effects of a PPARgamma agonist, darglitazone, on bone in mice. Bone 39 (2006) 796-806
95. Schwartz A.V., Sellmeyer D.E., Vittinghoff E., Palermo L., Lecka-Czernik B., Feingold K.R., et al. Thiazolidinedione use and bone loss in older diabetic adults. J Clin Endocrinol Metab 91 (2006) 3349-3354
96. Kahn S.E., Haffner S.M., Heise M.A., Herman W.H., Holman R.R., Jones N.P., et al. Glycemic durability of rosiglitazone, retformin, or glyburide monotherapy. N Engl J Med 355 (2006) 2427-2443
97. Pedrazzoni M., Ciotti G., Pioli G., Girasole G., Davoli L., Palummeri E., et al. Osteocalcin levels in diabetic subjects. Calcif Tissue Int 45 (1989) 331-336
98. Rico H., Hernandez E.R., Cabranes J.A., and Gomez-Castresana F. Suggestion of a deficient osteoblastic function in diabetes mellitus: the possible cause of osteopenia in diabetics. Calcif Tissue Int 45 (1989) 71-73
99. Achemlal L., Tellal S., Rkiouak F., Nouijai A., Bezza A., Derouiche el M., et al. Bone metabolism in male patients with type 2 diabetes. Clin Rheumatol 24 (2005) 493-496
100. Loder R.T. The influence of diabetes mellitus on the healing of closed fractures. Clin Orthop Relat Res 232 (1988) 210-216
101. Carnevale V., Romagnoli E., and D'Erasmo E. Skeletal involvement in patients with diabetes mellitus. Diabetes Metab Res Rev 20 (2004) 196-204
102. Bouillon R. Diabetic bone disease. Calcif Tissue Int 49 (1991) 155-160
103. Collin P., Kaukinen K., Valimaki M., and Salmi J. Endocrinological disorders and celiac disease. Endocr Rev 23 (2002) 464-483
104. He H., Liu R., Desta T., Leone C., Gerstenfeld L.C., and Graves D.T. Diabetes causes decreased osteoclastogenesis, reduced bone formation, and enhanced apoptosis of osteoblastic cells in bacteria stimulated bone loss. Endocrinology 145 (2004) 447-452
105. Shimoaka T., Kamekura S., Chikuda H., Hoshi K., Chung U.-I., Akune T., et al. Impairment of bone healing by insulin receptor substrate-1 deficiency. J Biol Chem 279 (2004) 15314-15322
106. Akune T., Ogata N., Hoshi K., Kubota N., Terauchi Y., Tobe K., et al. Insulin receptor substrate-2 maintains predominance of anabolic function over catabolic function of osteoblasts. J Cell Biol 159 (2002) 147-156
107. Thomas D.M., Udagawa N., Hards D.K., Quinn J.M.W., Moseley J.M., Findlay D.M., et al. Insulin receptor expression in primary and cultured osteoclast-like cells. Bone 23 (1998) 181
108. Dixit P.K., and Ekstrom R.A. Decreased breaking strength of diabetic rat bone and its improvement by insulin treatment. Calcif Tissue Int. 32 (1980) 195-199
109. Goodman W.G., and Hori M.T. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes 33 (1984) 825-831
110. Yamagishi S., Nakamura K., and Inoue H. Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Med Hypotheses 65 (2005) 1013-1015
111. Katayama Y., Akatsu T., Yamamoto M., Kugai N., and Nagata N. Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia. J Bone Miner Res 11 (1996) 931-937
112. Alikhani M., Alikhani Z., Boyd C., MacLellan C.M., Raptis M., Liu R., et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40 (2007) 345
113. Miyata T., Notoya K., Yoshida K., Horie K., Maeda K., Kurokawa K., et al. Advanced glycation end products enhance osteoclast-induced bone resorption in cultured mouse unfractionated bone cells and in rats implanted subcutaneously with devitalized bone particles. J Am Soc Nephrol 8 (1997) 260-270
114. Santana R.B., Xu L., Chase H.B., Amar S., Graves D.T., and Trackman P.C. A role for advanced glycation end products in diminished bone healing in type 1 diabetes. Diabetes 52 (2003) 1502-1510
115. Simonet W.S., Lacey D.L., Dunstan C.R., Kelley M., Chang M.S., Luthy R., et al. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89 (1997) 309
116. Galluzzi F., Stagi S., Salti R., Toni S., Piscitelli E., Simonini G., et al. Osteoprotegerin serum levels in children with type 1 diabetes: a potential modulating role in bone status. Eur J Endocrinol 153 (2005) 879-885
117. Browner W.S., Lui L.Y., and Cummings S.R. Associations of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures, and mortality in elderly women. J Clin Endocrinol Metab 86 (2001) 631-637
118. Ivers R.Q., Cumming R.G., Mitchell P., and Peduto A.J. Diabetes and risk of fracture: the blue mountains eye study. Diabetes Care 24 (2001) 1198-1203
119. Brown J.P., and Josse R.G. 2002 clinical practice guidelines for the diagnosis and management of osteoporosis in Canada. CMAJ 167 (2002) 1S-34S
120. Pascual J., Argente J., Lopez M.B., Munoz M., Martinez G., Vazquez M.A., et al. Bone mineral density in children and adolescents with diabetes mellitus type 1 of recent onset. Calcif Tissue Int 62 (1998) 31-35
121. Ingberg C.M., Palmer M., Aman J., Arvidsson B., Schvarcz E., and Berne C. Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255 (2004) 392-398
122. Gerdhem P., Isaksson A., Akesson K., and 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 16 (2005) 1506-1512