Bone disease in diabetes

Current Diabetes Reviews

Volumn 6, Issue 3, 2010, Pages 144-155

  Isidro, Ma Luisa ^a   Ruano, Belén ^a  

^a HOSPITAL JUAN CANALEJO   (Spain)

Author keywords

Bone mineral density; Diabetes; Fracture; Osteopenia; Osteoporosis

Indexed keywords

ADIPOCYTOKINE; ADIPONECTIN; ADVANCED GLYCATION END PRODUCT; ALENDRONIC ACID; AMYLIN; ANTICOAGULANT AGENT; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; COLLAGEN; DIGOXIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; GLIBENCLAMIDE; GLITAZONE DERIVATIVE; GROWTH HORMONE; HEMOGLOBIN A1C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN; LEPTIN; METFORMIN; NITRATE; PAMIDRONIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PIOGLITAZONE; ROSIGLITAZONE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; THIAZIDE DIURETIC AGENT; VITAMIN D;

ADRENERGIC SYSTEM; ARTICLE; BODY FAT DISTRIBUTION; BONE DENSITY; BONE DESTRUCTION; BONE DISEASE; BONE MASS; BONE MINERALIZATION; BONE REMODELING; BONE TURNOVER; CALCIUM ABSORPTION; CALCIUM BALANCE; CALCIUM BLOOD LEVEL; CALCIUM HOMEOSTASIS; CALCIUM URINE LEVEL; CLINICAL TRIAL; COMORBIDITY; DIABETES MELLITUS; DIABETIC MICROANGIOPATHY; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC PATIENT; DIABETIC RETINOPATHY; EXERCISE; FALLING; FEMUR; FRACTURE; GROWTH HORMONE RELEASE; HEMOGLOBIN BLOOD LEVEL; HIP FRACTURE; HORMONE SUBSTITUTION; HUMAN; HUMERUS FRACTURE; HYPERGLYCEMIA; HYPERINSULINISM; HYPOGONADISM; HYPOINSULINEMIA; INFLAMMATION; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; INSULIN TREATMENT; LUMBAR SPINE; METABOLIC REGULATION; NEUROPATHIC JOINT DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PATHOPHYSIOLOGY; POSTMENOPAUSE; PRIORITY JOURNAL; RADIUS; SECONDARY HYPERPARATHYROIDISM; SIGNAL TRANSDUCTION; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY;

BONE DENSITY; BONE DISEASES, METABOLIC; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FRACTURES, BONE; HUMANS; RISK FACTORS;

EID: 77952852099     PISSN: 15733998     EISSN: None     Source Type: Journal    
DOI: 10.2174/157339910791162970     Document Type: Article

References (201)

1. 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: 495-505.
2. Hampson G, Evans C, Petitt RJ, et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia 1998; 41: 1314-20.
3. 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: 399-403.
4. 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: 297-306.
5. Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. Bone loss and bone turnover in diabetes. Diabetes 1995; 44: 775-82.
6. Tuominen JT, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 1999; 22: 1196-200.
7. Forst T, Pfützner A, Kann P, et al. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 1995; 12: 874-9.
8. 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: 295-303.
9. 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 Complicat 2006; 20: 302-7.
10. 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: 306-11.
11. 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: 1729-35.
12. Thrailkill KM, Lumpkin CK Jr, Bunn RC, Kemp SF, Fowlkes JL. Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 2005; 289: E735-45.
13. Räkel A, Sheehy O, Rahme E, LeLorier J. Osteoporosis among patients with type 1 and type 2 diabetes. Diabetes Metab 2008; 34: 193-205.
14. Miazgowski T, Czekalski S. A 2-year follow-up study of bone mineral density and markers of bone turnover in patients with long-standing insulin-dependent diabetes mellitus. Osteoporos Int 1998; 8: 399-403.
15. Gunczler P, Lanes R, Paz-Martinez 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 1998; 11: 413-9.
16. López-Ibarra PJ, Pastor MM, Escobar-Jiménez F, et al. Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract 2001; 7: 346-51.
17. Bonfanti R, Mora S, Prinster C, et al. Bone modeling indexes at onset and during the first year of follow-Up in insulin-dependent diabetic children. Calcif Tissue Int 1997; 60: 397-400.
18. De Schepper J, Smitz J, Rosseneu S, Bollen P, Louis O. Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 1998; 50: 193-6.
19. Valerio G, del Puente A, Esposito-del Puente A, Buono P, Mozzillo E, Franzese A. The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 2002; 58: 266-72.
20. Ersoy B, Gök en D, Darcan S, Mavi E, Oztürk C. Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 1999; 66: 375-9.
21. 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: 56-62.
22. 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: 627-34.
23. Hui SL, Epstein S, Johnston CC Jr. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab 1985; 60: 74-80.
24. 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: 173-5.
25. Campos Pastor MM, López-Ibarra PJ, Escobar-Jiménez F, Serrano Pardo MD, García-Cervigón AG. Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int 2000; 11: 455-9.
26. 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: 409-14.
27. Kwon DJ, Kim JH, Chung KW, Kim JH, Lee JW, Kim SP, Lee HY. 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: 157-62.
28. 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: 317-21.
29. De Liefde II, van der Klift M, de Laet CEDH, van Daele PLA, Hofman A, Pols HAP. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 2005; 16: 1713-20.
30. 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: 688-98.
31. Hanley DA, Brown JP, Tenenhouse A, et al. Canadian Multicentre Osteoporosis Study Research Group. 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: 784-90.
32. Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, 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: 1963-8.
33. Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 1992; 268: 3333-7.
34. Gerdhem P, Isaksson A, Akesson K, Obrant KJ. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 2005; 16: 1506-12.
35. Schwartz AV, Sellmeyer DE, Strotmeyer ES, et al. Health ABC Study. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 2005; 20: 596-603.
36. Dobnig H, Piswanger-Sölkner 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: 3355-63.
37. Strotmeyer ES, Cauley JA, Schwartz AV, et al. Health ABC Study. 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: 1084-91.
38. 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: 19-29.
39. Achemlal L, Tellal S, Rkiouak F, et al. Bone metabolism in male patients with type 2 diabetes. Clin Rheumatol 2005; 24: 493-6.
40. El Miedany YM, El Gaafary S, El Baddini MA. Osteoporosis in older adults with non-insulin-dependent diabetes mellitus: is it sex related? Clin Exp Rheumatol 1999; 17: 561-7.
41. Erba ci AB, Araz M, Erba ci A, Tarakçio lu M, Namiduru ES. Serum prolidase activity as a marker of osteoporosis in type 2 diabetes mellitus. Clin Biochem 2002; 35: 263-8.
42. Cakatay U, Telci A, Kayali R, Akçay T, Sivas A, Aral F. Changes in bone turnover on deoxypyridinoline levels in diabetic patients. Diabetes Res Clin Pract 1998; 40: 75-9.
43. Oz SG, Guven GS, 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: 1598-604.
44. Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yano S, Sugimoto T. Combination of obesity with hyperglycemia is a risk factor for the presence of vertebral fractures in type 2 diabetic men. Calcif Tissue Int 2008; 83: 324-31.
45. 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: 29-33.
46. Okazaki R, Totsuka Y, Hamano K, et al. Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 1997; 82: 2915-20.
47. Bouillon R, Bex M, Van Herck E, et al. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab 1995; 80: 1194-202.
48. Shires R, Teitelbaum SL, Bergfeld MA, Fallon MD, Slatopolsky E, Avioli LV. The effect of streptozotocin-induced chronic diabetes mellitus on bone and mineral homeostasis in the rat. J Lab Clin Med 1981; 97: 231-40.
49. Goodman WG, Hori MT. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes 1984; 33: 825-31.
50. Mishima N, Sahara N, Shirakawa M, Ozawa H. Effect of streptozotocin-induced diabetes mellitus on alveolar bone deposition in the rat. Arch Oral Biol 2002; 47: 843-9.
51. McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem 2007; 102: 1343-57.
52. Irwin R, Lin HV, Motyl KJ, McCabe LR. Normal bone density obtained in the absence of insulin receptor expression in bone. Endocrinology 2006; 147: 5760-7.
53. Fulzele K, DiGirolamo DJ, Liu Z, Xu J, Messina JL, Clemens TL. Disruption of the insulin-like growth factor type 1 receptor in osteoblasts enhances insulin signaling and action. J Biol Chem 2007; 282: 25649-58.
54. Bravenboer N, Holzmann P, de Boer H, Roos JC, van der Veen EA, Lips P. The effect of growth hormone (GH) on histomorphometric indices of bone structure and bone turnover in GH-deficient men. J Clin Endocrinol Metab 1997; 82: 1818-22.
55. Baum HB, Biller BM, Finkelstein JS, et al. Effects of physiologic growth hormone therapy on bone density and body composition in patients with adult-onset growth hormone deficiency. A randomized, placebo-controlled trial. Ann Intern Med 1996; 125: 883-90.
56. Johansson AG, Engström BE, Ljunghall S, Karlsson FA, Burman P. Gender differences in the effects of long term growth hormone (GH) treatment on bone in adults with GH deficiency. J Clin Endocrinol Metab 1999; 84: 2002-7.
57. Amato G, Carella C, Fazio S, et al. Body composition, bone metabolism, and heart structure and function in growth hormone (GH)-deficient adults before and after GH replacement therapy at low doses. J Clin Endocrinol Metab 1993; 77: 1671-6.
58. Willemsen RH, Arends NJ, Bakker-van Waarde WM, et al. Long-term effects of growth hormone (GH) treatment on body composition and bone mineral density in short children born small-for-gestational-age: six-year follow-up of a randomized controlled GH trial. Clin Endocrinol (Oxf) 2007; 67: 485-92.
59. Ali O, Shim M, Fowler E, et al. Growth hormone therapy improves bone mineral density in children with cerebral palsy: a preliminary pilot study. J Clin Endocrinol Metab 2007; 92: 932-7.
60. Tangpricha V, Luo M, Fernández-Estívariz C, et al. Growth hormone favorably affects bone turnover and bone mineral density in patients with short bowel syndrome undergoing intestinal rehabilitation. J Parenter Enteral Nutr 2006; 30: 480-6.
61. Kim JG, Shin CS, Choi YM, Moon SY, Kim SY, Lee JY. The relationship among circulating insulin-like growth factor components, biochemical markers of bone turnover and bone mineral density in postmenopausal women under the age of 60. Clin Endocrinol (Oxf) 1999; 51: 301-7.
62. Landin-Wilhelmsen K, Nilsson A, Bosaeus I, Bengtsson BA. Growth hormone increases bone mineral content in postmenopausal osteoporosis: a randomized placebo-controlled trial. J Bone Miner Res 2003; 18: 393-405.
63. Kassem M, Brixen K, Blum WF, Mosekilde L, Eriksen EF. Normal osteoclastic and osteoblastic responses to exogenous growth hormone in patients with postmenopausal spinal osteoporosis. J Bone Miner Res 1994; 9: 1365-70.
64. Holloway L, Butterfield G, Hintz RL, Gesundheit N, Marcus R. Effects of recombinant human growth hormone on metabolic indices, body composition, and bone turnover in healthy elderly women. J Clin Endocrinol Metab 1994; 79: 470-9.
65. Yamaguchi T, Kanatani M, Yamauchi M, et al. Serum levels of insulin-like growth factor (IGF); IGF-binding proteins-3, -4, and - 5; and their relationships to bone mineral density and the risk of vertebral fractures in postmenopausal women. Calcif Tissue Int 2006; 78: 18-24.
66. Yakar S, Rosen CJ, Beamer WG, et al. Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest 2002; 110: 771-81.
67. Yakar S, Bouxsein ML, Canalis E, et al. The ternary IGF complex influences postnatal bone acquisition and the skeletal response to intermittent parathyroid hormone. J Endocrinol 2006; 189: 289-99.
68. Chiarelli F, Giannini C, Mohn A. Growth, growth factors and diabetes. Eur J Endocrinol. 2004 Nov; 151 Suppl 3:U109-17.
69. 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: 316-9.
70. Ward DT, Yau SK, Mee AP, et al. Functional, molecular, and biochemical characterization of streptozotocin-induced diabetes. J Am Soc Nephrol 2001; 12: 779-90.
71. Nyomba BL, Verhaeghe J, Thomasset M, Lissens W, Bouillon R. Bone mineral homeostasis in spontaneously diabetic BB rats. I. Abnormal vitamin D metabolism and impaired active intestinal calcium absorption. Endocrinology 1989; 124: 565-72.
72. Schneider LE, Schedl HP, McCain T, Haussler MR. Experimental diabetes reduces circulating 1,25-dihydroxyvitamin D in the rat. Science 1977; 196: 1452-4.
73. Malone JI, Lowitt S, Duncan JA, Shah SC, Vargas A, Root AW. Hypercalciuria, hyperphosphaturia, and growth retardation in children with diabetes mellitus. Pediatrics 1986; 78: 298-304.
74. Gunczler P, Lanes R, Esaa S, Paoli M. Effect of glycemic control on the growth velocity and several metabolic parameters of conventionally treated children with insulin dependent diabetes mellitus. J Pediatr Endocrinol Metab 1996; 9: 569-75.
75. Périmenis P, Wémeau JL, Vantyghem MC. Hypercalciuria. Ann Endocrinol (Paris) 2005; 66: 532-9.
76. Thalassinos NC, Hadjiyanni P, Tzanela M, Alevizaki C, Philokiprou D. Calcium metabolism in diabetes mellitus: effect of improved blood glucose control. Diabet Med 1993; 10: 341-4.
77. Gregorio F, Cristallini S, Santeusanio F, Filipponi P, Fumelli P. Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract 1994; 23: 43-54.
78. Holick MF, Chen TC. Vitamin D deficiency: a worldwide problem with health consequences. Am J Clin Nutr 2008; 87: 1080S-6S.
79. Pozzilli P, Manfrini S, Crinò A, et al. IMDIAB group. Low levels of 25-hydroxyvitamin D3 and 1,25-dihydroxyvitamin D3 in patients with newly diagnosed type 1 diabetes. Horm Metab Res 2005; 37: 680-3.
80. Littorin B, Blom P, Schölin A, et al. Lower levels of plasma 25- hydroxyvitamin D among young adults at diagnosis of autoimmune type 1 diabetes compared with control subjects: results from the nationwide Diabetes Incidence Study in Sweden (DISS). Diabetologia 2006; 49: 2847-52.
81. Greer RM, Rogers MA, Bowling FG, et al. Australian children and adolescents with type 1 diabetes have low vitamin D levels. Med J Aust 2007; 187: 59-60.
82. Svoren BM, Volkening LK, Butler DA, Moreland EC, Anderson BJ, Laffel LM. Temporal trends in the treatment of pediatric type 1 diabetes and impact on acute outcomes. J Pediatr 2007; 150: 279-85.
83. Svoren BM, Volkening LK, Wood JR, Laffel LM. Significant vitamin D deficiency in youth with type 1 diabetes mellitus. J Pediatr 2009; 154: 132-4.
84. Ikeda K, Matsumoto T, Morita K, et al. The role of insulin in the stimulation of renal 1,25-dihydroxyvitamin D synthesis by parathyroid hormone in rats. Endocrinology 1987; 121: 1721-6.
85. Spencer EM, Khalil M, Tobiassen O. Experimental diabetes in the rat causes an insulin-reversible decrease in renal 25-hydroxyvitamin D3-1 alpha-hydroxylase activity. Endocrinology 1989; 107: 300-5.
86. Hough S, Fausto A, Sonn Y, Dong Jo OK, Birge SJ, Avioli LV. Vitamin D metabolism in the chronic streptozotocin-induced diabetic rat. Endocrinology 1983; 113: 790-6.
87. 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: 3622-31.
88. Zayzafoon M, Stell C, Irwin R, McCabe LR. Extracellular glucose influences osteoblast differentiation and c-Jun expression. J Cell Biochem 2000; 79: 301-10.
89. Botolin S, McCabe LR. Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem 2006; 99: 411-24.
90. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem 2006; 98: 251-66.
91. McCarthy AD, Uemura T, Etcheverry SB, Cortizo AM. Advanced glycation endproducts interefere with integrin-mediated osteoblastic attachment to a type-I collagen matrix. Int J Biochem Cell Biol 2004; 36: 840-8.
92. Kume S, Kato S, Yamagishi S, et al. Advanced glycation endproducts attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone. J Bone Miner Res 2005; 20: 1647-58.
93. Wolf G. Energy regulation by the skeleton. Nutr Rev 2008; 66: 229-33.
94. Isaia GC, D'Amelio P, Di Bella S, Tamone C. Is leptin the link between fat and bone mass? J Endocrinol Invest 2005; 28 (10 Suppl): 61-5.
95. Cirmanová V, Bayer M, Stárka L, Zajícková K. The effect of leptin on bone: an evolving concept of action. Physiol Res 2008; 57 (Suppl 1): S143-51.
96. Myers SE, Albert SG, Haas MJ, Clifton D, Mooradian AD. Pubertal changes in serum leptin levels in adolescents with type 1 diabetes mellitus: a controlled longitudinal study. J Pediatr Endocrinol Metab 2004; 17: 1653-62.
97. Karagüzel G, Ozdem S, Boz A, Bircan I, Akçurin S. Leptin levels and body composition in children and adolescents with type 1 diabetes. Clin Biochem 2006; 39: 788-93.
98. Kiess W, Anil M, Blum WF, et al. Serum leptin levels in children and adolescents with insulin-dependent diabetes mellitus in relation to metabolic control and body mass index. Eur J Endocrinol 1998; 138: 501-9.
99. Kassem HS, Arabi A, Zantout MS, Azar ST. Negative effect of leptin on bone mass in type 1 diabetes. Acta Diabetol 2008; 45: 237-41.
100. Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 1995; 332: 305-11.
101. Almawi WY, Tamim H, Azar ST. Clinical review 103: T helper type 1 and 2 cytokines mediate the onset and progression of type I (insulin-dependent) diabetes. J Clin Endocrinol Metab 1999; 84: 1497-502.
102. Rabinovitch A, Suarez-Pinzon WL. Role of cytokines in the pathogenesis of autoimmune diabetes mellitus. Rev Endocr Metab Disord 2003; 4: 291-9.
103. Greenberg AS, McDaniel ML. Identifying the links between obesity, insulin resistance and beta-cell function: potential role of adi-pocyte-derived cytokines in the pathogenesis of type 2 diabetes. Eur J Clin Invest 2002; 32 (Suppl 3): 24-34.
104. Alexandraki K, Piperi C, Kalofoutis C, Singh J, Alaveras A, Kalo-foutis A. Inflammatory process in type 2 diabetes: The role of cytokines. Ann N Y Acad Sci 2006; 1084: 89-117.
105. Pankewycz OG, Guan JX, Benedict JF. Cytokines as mediators of autoimmune diabetes and diabetic complications. Endocr Rev 1995; 16: 164-76.
106. Schrijvers BF, De Vriese AS, Flyvbjerg A. From hyperglycemia to diabetic kidney disease: the role of metabolic, hemodynamic, intracellular factors and growth factors/cytokines. Endocr Rev 2004; 25: 971-1010.
107. Devaraj S, Glaser N, Griffen S, Wang-Polagruto J, Miguelino E, Jialal I. Increased monocytic activity and biomarkers of inflammation in patients with type 1 diabetes. Diabetes 2006; 55: 774-9.
108. Jeffcoate WJ, Game F, Cavanagh PR. The role of proinflammatory cytokines in the cause of neuropathic osteoarthropathy (acute Charcot foot) in diabetes. Lancet 2005; 366: 2058-61.
109. Horcajada-Molteni MN, Chanteranne B, Lebecque P, et al. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J Bone Miner Res 2001; 16: 958-65.
110. Romero DF, Bryer HP, Rucinski B, et al. Amylin increases bone volume but cannot ameliorate diabetic osteopenia. Calcif Tissue Int 1995; 56: 54-61.
111. Vogt MT, Cauley JA, Kuller LH, Nevitt MC. Bone mineral density and blood flow to the lower extremities: the study of osteoporotic fractures. J Bone Miner Res 1997; 12: 283-9.
112. Wong SY, Kwok T, Woo J, et al. Bone mineral density and the risk of peripheral arterial disease in men and women: results from Mr. and Ms Os, Hong Kong. Osteoporos Int 2005; 16: 1933-8.
113. Amir G, Rosenmann E, Sherman Y, Greenfeld Z, Ne'eman Z, Cohen AM. Osteoporosis in the Cohen diabetic rat: correlation between histomorphometric changes in bone and microangiopathy. Lab Invest 2002; 82: 1399-405.
114. Scragg R, Holdaway I, Singh V, Metcalf P, Baker J, Dryson E. Serum 25-hydroxyvitamin D3 levels decreased in impaired glucose tolerance and diabetes mellitus. Diabetes Res Clin Pract 1995; 27: 181-8.
115. Inaba M, Nishizawa Y, Mita K, et al. Poor glycemic control impairs the response of biochemical parameters of bone formation and resorption to exogenous 1,25-dihydroxyvitamin D3 in patients with type 2 diabetes. Osteoporos Int 1999; 9: 525-31.
116. Chang-Quan H, Bi-Rong D, Ping H, Zhen-Chan L. Insufficient renal 1-alpha hydroxylase and bone homeostasis in aged rats with insulin resistance or type 2 diabetes mellitus. J Bone Miner Metab 2008; 26: 561-8.
117. Reid IR. Relationships among body mass, its components, and bone. Bone 2002; 31: 547-55.
118. Ensrud KE, Lipschutz RC, Cauley JA, et al. Body size and hip fracture risk in older women: a prospective study. Study of Osteoporotic Fractures Research Group. Am J Med 1997; 103: 274-80.
119. De Laet C, Kanis JA, Odén A, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 2005; 16: 1330-8.
120. Bridges MJ, Moochhala SH, Barbour J, Kelly CA. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol 2005; 42: 82-6.
121. Reid IR, Cornish J, Baldock PA. Nutrition-related peptides and bone homeostasis. J Bone Miner Res 2006; 21: 495-500.
122. Yamaguchi T, Kanazawa I, Yamamoto M, et al. Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone. 2009; 45: 174-9.
123. Schäffler A, Müller-Ladner U, Schölmerich J, Büchler C. Role of adipose tissue as an inflammatory organ in human diseases. Endocr Rev 2006; 27: 449-67.
124. Crepaldi G, Romanato G, Tonin P, Maggi S. Osteoporosis and body composition. J Endocrinol Invest 2007; 30 (6 Suppl): 42-7.
125. 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: 623-8.
126. Lenchik L, Register TC, Hsu FC, et al. Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 2003; 33: 646-51.
127. Jürimäe J, Jürimäe T, Leppik A, Kums T. The influence of ghrelin, adiponectin, and leptin on bone mineral density in healthy postmenopausal women. J Bone Miner Metab 2008; 26: 618-23.
128. Gonnelli S, Caffarelli C, del Santo K, et al. The relationship of ghrelin and adiponectin with bone mineral density and bone turnover markers in elderly men. Calcif Tissue Int 2008; 83: 55-60.
129. Zoico E, Zamboni M, Di Francesco V, et al. Relation between adiponectin and bone mineral density in elderly post-menopausal women: role of body composition, leptin, insulin resistance, and dehydroepiandrosterone sulfate. J Endocrinol Invest 2008; 31: 297-302.
130. Kanazawa I, Yamaguchi T, Yamauchi M, et al. Adiponectin is associated with changes in bone markers during glycemic control in Type 2 Diabetes Mellitus. J Clin Endocrinol Metab 2009; 94: 3031-7.
131. Dhindsa S, Prabhakar S, Sethi M, Bandyopadhyay A, Chaudhuri A, Dandona P. Frequent occurrence of hypogonadotropic hypogonadism in type 2 diabetes. J Clin Endocrinol Metab 2004; 89: 5462-8.
132. Dhindsa S, Bhatia V, Dhindsa G, Chaudhuri A, Gollapudi GM, Dandona P. The effects of hypogonadism on body composition and bone mineral density in type 2 diabetic patients. Diabetes Care 2007; 30: 1860-1.
133. Christensen JO, Svendsen OL. Bone mineral in pre- and postmeno- pausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int 1999; 10: 307-11.
134. Hadjidakis DJ, Mylonakis AM, Sfakianakis ME, Raptis AE, Raptis SA. Diabetes and premature menopause: is their co-existence detrimental to the skeleton? Eur J Endocrinol 2005; 152: 437-42.
135. McNair P, Christensen MS, Madsbad S, Christiansen C, Transbøl I. Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 1981; 96: 81-6.
136. Heath H 3rd, Lambert PW, Service FJ, Arnaud SB. Calcium homeostasis in diabetes mellitus. J Clin Endocrinol Metab 1979; 49: 462-6.
137. 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: 409-14.
138. Heath H, Melton LJ, Chu CP. Diabetes mellitus and risk of skeletal fracture. N Engl J Med 1980; 303: 567-70.
139. Strotmeyer ES, Cauley JA, Schwartz AV, et al. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults. The Health, Aging and Body Composition Study. Arch Intern Med 2005; 165: 1612-7.
140. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - a meta-analysis. Osteoporos Int 2007; 18: 427-44.
141. Bonds DE, Larson JC, Schwartz AV, et al. Risk of fracture in women with type 2 diabetes: the Womeńs Health Initiative Observational Study. J Clin Endocrinol Metab 2006; 91: 3404-10.
142. Janghorbani M, Feskanich D, Willett WC, Hu F. Prospective Study of diabetes and risk of hip fracture: the Nurseś Health Study. Diabetes Care 2006; 29: 1573-8.
143. Ivers RQ, Cumming RG, Mitchell P, Peduto AJ. Diabetes and risk of fracture: the Blue Mountains Eye Study. Diabetes Care 2001; 24: 1198-203.
144. Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 2001; 24: 1192-7.
145. Miao J, Brismar K, Nyrén O, Ugarph-Morawski A, Weimin Y. Elevated hip fracture risk in type 1 diabetic patients: a population- based cohort study in Sweeden. Diabetes Care 2005; 28: 2850-5.
146. Lipscombe LL, Jamai SA, Booth GL, Hawker GA. The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care 2007; 30: 835-41.
147. Holmberg AH, Nilsson PM, Nilsson JA, Akesson K. The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women. J Clin Endocrinol Metab 2008; 93: 815-22.
148. Sosa M, Saavedra P, Jódar E, et al. GIUMO Study Group. Bone mineral density and risk of fractures in aging, obese postmenopausal women with type 2 diabetes. The GIUMO Study. Aging Clin Exp Res 2009; 21: 27-32.
149. Melton LJ 3rd, Leibson CL, Achenbach SJ, Therneau TM, Khosla S. Fracture risk in type 2 diabetes: update of a population-based study. J Bone Miner Res 2008; 23: 1334-42.
150. Wolf SK. Diabetes mellitus and predisposition to athletic pedal fracture. J Foot Ankle Surg 1998; 37:16-22.
151. El-Khoury G, Kathol MH. Neuropathic fractures in patients with diabetes mellitus. Radiology 1980; 134: 313-6.
152. Cundy TF, Edmons ME, Watkins RJ. Osteopenia and metatarsal fractures in diabetic neuropathy. Diabet Med 1985; 2: 461-4.
153. Gill G, Benbow S, Tesfaye S, Kaczmaczyk E, Kaye L. Painless stress fractures in diabetic neuropathic feet. Postgrad Med J 1997; 73: 241-2.
154. Verhaeghe J, Suiker AM, Einhorn TA, et al. Brittle bones in spontaneously diabetic female rats cannot be predicted by bone mineral measurements: studies in diabetic and ovariectomized rats. J Bone Miner Res 1994; 9: 1657-67.
155. Vashishth D. The role of the collagen matrix in skeletal fragility. Curr Osteopor Rep 2007; 5: 62-6.
156. Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T. Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 2008; 93: 1013-9.
157. Schwartz AV, Garnero P, Hillier TA, et al. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 2009: 94: 2380-6.
158. Saito M, Maruma K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Ostoporos Int 2010; 21(2): 195-214.
159. Kahn SE, Haffner SM, Heise MA, et al. Glycemic durability of rosiglitazone, metformin or glyburide monotherapy. N Engl J Med 2006; 355: 2427-43.
160. Schwartz AV, Sellmeyer DE, Vittinghoff E, et al. Thiazolidinedione use and bone loss in older diabetic adults. J Clin Endocrinol Metab 2006; 91: 3349-54.
161. Kahn SE, Zinman B, Lachin JM, et al. Rosiglitazon-associatedfractures in type 2 diabetes. An analysis from a Diabetes Outcome Progression Trial (ADOPT). Diabetes Care 2008; 31: 845-51.
162. Schwartz AV. Thiazolidinedione therapy gets complicated: is bone loss the price of improved insulin resistance? Diabetes Care 2007; 6: 1670-1.
163. Schwartz AV. Diabetes, TZDs and bone: a review of the clinical evidence. PPAR Res 2006; 24502.
164. Monami M, Cresci B, Colombini A, et al. Bone fractures and hypoglycemic treatment in type 2 diabetic patients. Diabetes Care 2008; 31: 199-203.
165. Rejnmark L. Bone effects of glitazones and other anti-diabetic drugs. Curr Drug Saf 2008; 3: 194-8.
166. McDonough AK, Rosenthal RS, Cao X, Saag KG. The effect of thiazolidinediones on BMD and osteoporosis. Nat Clin Pract Endocrinol Metab 2008; 4: 507-13.
167. Rizos CV, Elisaf MS, Mikhailidis DP, Liberopoulos EN. How safe is the use of thiazolidinediones in clinical practice? Expert Opin Drug Saf 2009; 8: 15-32.
168. Vestergaard P. Bone metabolism in type 2 diabetes and role of thiazolidinediones. Curr Opin Endocrinol Diabetes Obes 2009; 16: 125-31.
169. 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: 2792-8.
170. Schwartz A. TZDs and bone: a review of the recent clinical evidence. PPAR Research 2008; 297893.
171. Loke YK, Singh S, Furberg CD. Long-term use of thiazolidinediones and fractures in type 2 diabetes: a meta-analysis. CMAJ 2009; 180: 32-9.
172. Forsén L, Meyer HE, Midthjell K, Edna TH. Diabetes mellitus and the incidence of hip fractures: results from the Nord-Troudelarg Health Survey. Diabetologia 1999; 42: 920-5.
173. Jadhav SB, Jain GK. Statins and osteoporosis: new role for old drugs. J Pharm Pharmacol 2006; 58: 3-18.
174. Tang QO, Tran GT, Gamie Z, et al. Statins: under investigation for increasing bone mineral density and augmenting fracture healing. Expert Opin Investig Drugs 2008; 17: 1435-63.
175. Uzzan B, Cohen R, Nicolas P, Cucherat M, Perret GY. Effects of statins on bone mineral density: a metaanalysis of clinical studies. Bone 2007; 40: 1581-7.
176. Rejnmark L. Cardiovascular drugs and bone. Curr Drug Saf 2008; 3: 178-84.
177. Malmivaara A, Heliövaara M, Knekt P, Reunanen A, Aromaa A. Risk factors for injurious falls leading to hospitalization or death in a cohort of 19.500 adults. Am J Epidemiol 1993; 138: 384-94.
178. Gregg EW, Beckles GLA, Williamson DF, et al. Diabetes and physical disability among older U.S. adults. Diabetes Care 2000; 23: 1272-7.
179. Nelson DA, Jacober SJ. Why do older women with diabetes have an increased fracture risk? J Clin Endocrinol Metab 2001; 86: 29-31.
180. Brown SA, Sharpless JL. Osteoporosis: an under-appreciated complication of diabetes. Clin Diabetes 2004; 22: 10-2.
181. Lee JS, Kwok T, Leung PC, Woo J. Medical illnesses are more important than medications as risk factors of falls in older community dwellers? A cross-sectional study. Age Ageing 2006; 35: 246-51.
182. Maurer MS, Burcham J, Cheng H. Diabetes mellitus is associated with an increased risk of falls in elderly residents of a long-term care facility. J Gerontol A Biol Sci Med Sci 2005; 9: 1157-62.
183. Tinetti ME, Speechley M, Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med 1988; 319: 1701-7.
184. Schwartz AV, Hillier TA, Aellmeyer DE, et al. Older women with diabetes have a higher risk of falls: a prospective study. Diabetes Care 2002; 25: 1749-54.
185. Patel S, Hyer S, Tweed K, et al. Risk factors for fractures and falls in older women with type 2 diabetes mellitus. Calcif Tissue Int 2008; 82: 87-91.
186. Volpato S, Leveille SG, Blaum C, Fried LP, Guralnik JM. Risk factors for falls in older disabled women with diabetes: The Womeńs Health and Aging Study. J Gerontol A Biol Sci Med Sci 2005; 12: 1539-45.
187. 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.
188. Schwartz AV, Vittinghoff E, Sellmeyer DE, et al. Diabetes-related complications, glycemic control, and falls in older adults. Diabetes Care 2008; 31: 391-6.
189. Quandt SA, Stafford JM, Bell RA, Smith SL, Snively BM, Arcury TA. Predictors of falls in a multiethnic population of older rural adults with diabetes. J Gerontol A Biol Sci Med Sci 2006; 61: 394-8.
190. Bischoff HA, Stahelin HB, Dick W, et al. Effects of vitamin D and calcium supplementation on falls. A randomized controlled trial. J Bone Miner Res 2003; 18: 343-51.
191. Faulkner KA, Cauley JA, Zmuda JM, et al. Higher 1,25 dihy- droxyvitamin D3 concentrations associated with lower falls rates in older community-dwelling women. Osteoporos Int 2006; 17: 1318-28.
192. Chau DL, Edelman SV, Chandran M. Osteoporosis and diabetes. Curr Diab Rep 2003; 3: 37-42.
193. Chau DL, Goldstein-Fuchs J, Edelman SV. Osteoporosis among patients with diabetes: an overlooked disease. Diabetes Spectrum 2003; 16: 176-9.
194. Institute of Medicine: DRI: Dietary Reference Intakes for Calcium, Phosphorus, Magnesium, Vitamin D, and fluoride. Washington, D.C. National Academy Press, 1999.
195. Kannus P, Parkkari J, Niemi S, et al. Prevention of hip fractures in elderly people with use of a hip protector. N Engl J Med 2000; 34: 1506-13.
196. Kannus P, Parkkari J. Prevention of hip fracture with hip protectors. Age Ageing 2006; 35 (Suppl 2): 51-54.
197. Keegan THM, Schwartz AV, Bauer DC, Selolmeyer DE, Kelsey JL. Effect of alendronate on bone mineral density and biochemical markers of bone turnover in type 2 diabetic women. The Fracture Intervention Trial. Diabetes Care 2004; 27: 1547-53.
198. Jude EB, Selby PL, Lilleystone P, et al. Biphosphonates in the treatment of Charcot neuropathy: a double-blind randomised controlled trial. Diabetologia 2001; 44: 2032-7.
199. Dagdelen S, Sener D, Bayraktar M. Influence of type 2 diabetes mellitus on bone mineral density response to bisphosphonates in late postmenopausal osteoporosis. Adv Ther 2007; 24: 1314-20.
200. Barret-Connor E, Ensrud KE, Harper KD, et al. Post hoc analysis of data from the Multiple Outcomes of Raloxifene Evaluation (MORE) trial on the effect of 3 years on raloxifene treatment of glycemic control and cardiovascular disease risk factors in women with and without type 2 diabetes. Clin Ther 2003; 25: 919-30.
201. Ensrud KE, Cauley JA, Zhou L, Mason TM, Bowman PJ, Harper KD. Effect of raloxifene hydrochloride on bone mineral density and bone turnover markers in diabetic women: The Multiple Outcomes of Raloxifene Evaluation (MORE) trial. J Bone Miner Res 2001; 16 (Suppl 1): S415-27.