Type 1 diabetes and osteoporosis: A review of literature

Indian Journal of Endocrinology and Metabolism

Volumn 18, Issue 2, 2014, Pages 159-165

  Dhaon, Pooja ^a   Shah, Viral N ^b  

^a KING GEORGE'S MEDICAL UNIVERSITY   (India)

^b UNIVERSITY OF COLORADO DENVER   (United States)

Author keywords

Fracture risk; osteoporosis; type 1 diabetes

Indexed keywords

EID: 84995470840     PISSN: 22308210     EISSN: 22309500     Source Type: Journal    
DOI: 10.4103/2230-8210.129105     Document Type: Review

References (80)

1. Kalra S, Kalra B, Sharma A. Prevalence of type 1 diabetes mellitus in Karnal district, Haryana state, India. Diabetol Metab Syndr 2010;2:14.
2. Prasanna Kumar KM, Krishna P, Reddy SC, Gurrappa M, Aravind SR, Munichoodappa C. Incidence of type 1 diabetes mellitus and associated complications among children and young adults: results from Karnataka Diabetes Registry 1995-2008. J Indian Med Assoc 2008;106:708-11.
3. Ramachandran A, Snehalatha C, Krishnaswamy CV. The Incidence of IDDM in children in urban population in southern India. Madras South India. Diabetes Res Clin Pract 1996;34:79-82.
4. Ramachandran A, Snehalatha C, Khader O, Joseph TA, Visvanathan M. Prevalence of childhood diabetes in urban population in South India. Diabetes Res Clin Pract 1992;17:227-31.
5. Shah VN, Moser EG, Blau A, Dhingra M, Garg SK. The future of Basal insulin. Diabetes Technol Ther 2013;15:727-32.
6. Atkinson MA, Eisenbarth GS, Michels AW. Type 1 diabetes. Lancet 2013. [In press]
7. Miller RG, Secrest AM, Sharma RK, Songer TJ, Orchard TJ. Improvements in the life expectancy of type 1 diabetes: The Pittsburgh Epidemiology of Diabetes Complications study cohort. Diabetes 2012;61:2987-92.
8. Sue Kirkman M, Briscoe VJ, Clark N, Florez H, Haas LB, Halter JB, et al. Consensus Development Conference on Diabetes and Older Adults. Diabetes in older adults: A consensus report. J Am Geriatr Soc 2012;60:2342-56.
9. Albright F, Reifenstein EC. Bone development in diabetic children: A roentgen study. Am J Med Sci 1948;174:313-9.
10. Levin ME, Boisseau VC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med 1976;294:241-5.
11. Rosenbloom AL, Lezotte DC, Weber FT, Gudat J, Heller DR, Weber ML, et al. Diminution of bone mass in childhood diabetes. Diabetes 1977;26:1052-5.
12. Auwerx J, Dequeker J, Bouillon R, Geusens P, Nijs J. Mineral metabolism and bone mass at peripheral and axial skeleton in diabetes mellitus. Diabetes 1988;37:8-12.
13. Ponder SW, McCormick DP, Fawcett HD, Tran AD, Ogelsby GW, Brouhard BH, et al. Bone mineral density of the lumbar vertebrae in children and adolescents with insulin-dependent diabetes mellitus. J Pediatr 1992;120:541-5.
14. Olmos JM, Pérez-Castrillón JL, García MT, Garrido JC, Amado JA, González-Macías J. Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner 1994;26:1-8.
15. Gunczler P, Lanes R, Paz-Martinez V, Martinis R, Esaa S, Colmenares V. 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. 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.
17. Saha MT, Sievanen H, Salo MK, Tulokas S, Saha HH. Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int 2009;20:1401-6.
18. 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;20:302-7.
19. Hamilton EJ, Rakic V, Davis WA, Paul Chubb SA, Kamber N, Prince RL, et al. A five-year prospective study of bone mineral density in men and women with diabetes: The Fremantle Diabetes Study. Acta Diabetol 2012;49:153-8.
20. Liu EY, Wactawski-Wende J, Donahue RP, Dmochowski J, Hovey KM, Ouattrin T Does Low bone mineral density start in post-Teenage years in women with type 1 diabetes? Diabetes Care 2003 26 2365-9.
21. Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 2007;22:1317-28.
22. 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.
23. Joshi A, Varthakavi P, Chadha M, Bhagwat N. A study of bone mineral density and its determinants in type 1 diabetes. J Osteoporos 2013;2013:397814.
24. Roggen I, Gies I, Vanbesien J, Louis O, De Schepper J. Trabecular bone mineral density and bone geometry of the distal radius at completion of pubertal growth in childhood type 1 diabetes. Horm Res Paediatr 2013;79:68-74.
25. 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;20:302-7.
26. 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.
27. Lunt H, Florkowski CM, Cundy T, Kendall D, Brown LJ, Elliot JR, et al. A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes Res Clin Pract 1998;40:31-8.
28. López-Alvarenga JC, Zariñán T, Olivares A, González-Barranco J, Veldhuis JD, Ulloa-Aguirre A. Poorly controlled type I diabetes mellitus in young men selectively suppresses luteinizing hormone secretory burst mass. J Clin Endocrinol Metab 2002;87:5507-15.
29. Orwoll ES, Klein RF. Osteoporosis in men. Endocr Rev 1995;16:87-116.
30. 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.
31. Daga RA, Laway BA, Shah ZA, Mir SA, Kotwal SK, Zargar AH. High prevalence of vitamin D deficiency among newly diagnosed youth-onset diabetes mellitus in north India. Arq Bras Endocrinol Metabol 2012;56:423-8.
32. Borkar VV, Devidayal, Verma S, Bhalla AK. Low levels of vitamin D in North Indian children with newly diagnosed type 1 diabetes. Pediatr Diabetes 2010;11:345-50.
33. Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-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;58:31-9.
34. Rix M, Andreassen H, Eskildsen P. Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 1999;22:827-31.
35. Bouillon R. Diabetic bone disease. Calcif Tissue Int 1991;49:155-60.
36. Rejnmark L, Vestergaard P, Heickendorff L, Andreasen F, Mosekilala L. Loop diuretics increase bone turnover and decrease BMD in osteopenic postmenopausal women: Results from a randomized controlled study with bumetanide. J Bone Miner Res 2006;21:163-70.
37. Szypowska A, Bazik M, Groele L, Pankowska E. The prevalence of autoimmune thyroid disease and celiac disease in children and adolescents with type 1 diabetes mellitus. Pediatr Endocrinol Diabetes Metab 2008;14:221-4.
38. Lombardi F, Franzese A, Iafusco D, del Puente A, Esposito A, Prisco F, et al. Bone involvement in clusters of autoimmune diseases: Just a complication. Bone 2010;46:551-5.
39. Kota SK, Meher LK, Jammula S, Kota SK, Modi KD. Clinical profile of coexisting conditions in type 1 diabetes mellitus patients. Diabetes Metab Syndr 2012;6:70-6.
40. Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS. Increased fracture rates in Turners syndrome: A nationwide questionnaire survey. Clin Endocrinol (Oxf) 2003;59:89-96.
41. Horowitz M, Wishart JM, OLoughlin PD, Morris HA, Need AG, Nordin BE. Osteoporosis and Klinefelters syndrome. Clin Endocrinol (Oxf) 1992;36:113-8.
42. Saggese G, Baroncelli GI, Bertelloni S. Puberty and bone development. Best Pract Res Clin Endocrinol Metab 2002;16:53-64.
43. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR-gamma2transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 2004;3:379-89.
44. Lecka-Czernik B, Gubrij I, Moerman EJ, Kajkenova O, Lipschitz DA, Manolagas SC. Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARgamma2. J Cell Biochem 1999;74:357-71.
45. Botolin S, McCabe LR. Inhibition of PPAR-Gamma prevents type I diabetic bone marrow adiposity but not bone loss. J Cell Physiol 2006;209:967-76.
46. Bazelier MT, de Vries F, Vestergaard P, Herings RM, Gallagher AM, Leufkens HG, et al. Risk of fracture with thiazolidinediones: An individual patient data meta-Analysis. Front Endocrinol (Lausanne) 2013;4:11.
47. Habib ZA, Havstad SL, Wells K, Divine G, Pladevall M, Williams LK. Thiazolidinedione use and the longitudinal risk of fractures in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 2010;95:592-600.
48. Gopalakrishnan V, Vignesh RC, Arunakaran J, Aruldhas MM, Srinivasan N. Effects of glucose and its modulation by insulin and estradiol on BMSC differentiation into osteoblastic lineages. Biochem Cell Biol 2006;84:93-101.
49. Lu H, Kraut D, Gerstenfeld LC, Graves DT. Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology 2003;144:346-52.
50. Lechleitner M, Koch T, Herold M, Dzien A, Hoppichler F. Tumour necrosis factor-Alpha plasma level in patients with type 1 diabetes mellitus and its association with glycaemic control and cardiovascular risk. J Intern Med 2000;248:67-76.
51. Coe LM, Irwin R, Lippner D, McCabe LR. The bone marrow microenvironment contributes to type I diabetes induced osteoblast death. J Cell Physiol 2011;226:477-83.
52. Fraser JH, Helfrich MH, Wallace HM, Ralston SH. Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae. Bone 1996;19:223-6.
53. The effect of intensive treatment of diabetes on the development and progression of long-Term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993;329:977-86.
54. Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F. Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complications 2011;25:216-21.
55. Kim JH, Jung MH, Lee JM, Son HS, Cha BY, Chang SA. Diabetic peripheral neuropathy is highly associated with nontraumatic fractures in Korean patients with type 2 diabetes mellitus. Clin Endocrinol (Oxf) 2012;77:51-5
56. 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.
57. Sealand R, Razavi C, Adler RA. Diabetes mellitus and osteoporosis. Curr Diab Rep 2013;13:411-8.
58. Hamann C, Kirschner S, Günther KP, Hofbauer LC. Bone, sweet bone-osteoporotic fractures in diabetes mellitus. Nat Rev Endocrinol 2012;8:297-305.
59. Nixon AJ, Lillich JT, Burton-Wurster N, Lust G, Mohammad HO. Differentiated cellular function in fetal chondrocytes cultured with insulin-like growth factor-I and transforming growth factor-beta. J Orthop Res 1998;16:531-41.
60. Moyer-Mileur LJ, Slater H, Jordan KC, Murray MA. IGF-1 and IGF-binding proteins and bone mass, geometry, and strength: Relation to metabolic control in adolescent girls with type 1 diabetes. J Bone Miner Res 2008;23:188-91.
61. Horcajada-Molten MN, Chanteranne B, Lebecque P, Davicco MJ, Coxam V, Young A, et al. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J Bone Miner Res 2001;16:958-65.
62. Bhadada SK, Kochhar R, Bhansali A, Dutta U, Kumar PR, Poornachandra KS, et al. Prevalence and clinical profile of celiac disease in type 1 diabetes mellitus in north India. J Gastroenterol Hepatol 2011;26:378-81
63. Lucendo AJ, García-Manzanares A. Bone mineral density in adult coeliac disease: An updated review. Rev Esp Enferm Dig 2013;105:154-62.
64. Raisz LG. Clinical practice. Screening for osteoporosis. N Engl J Med 2005;353:164-71.
65. Gordon CM, Bachrach LK, Carpenter TO, Crabtree N, El-Hajj Fuleihan G, Kutilek S, et al. Dual energy x-ray absorptiometry interpretation and reporting in children and adolescents: The 2007 ISCD pediatric official positions. J Clin Densitom 2008;11:43-58.
66. Leib ES, Lewiecki EM, Binkley N, Hamdy RC. Official positions of the International Society for Clinical Densitometry. J Clin Densitom 2004;7:1-6.
67. Kalkwarf HJ, Zemel BS, Gilsanz V, Lappe JM, Horlick M, Oberfield S, et al. The Bone Mineral Density in Childhood Study (BMDCS): Bone mineral content and density according to age, sex, and race. J Clin Endocrinol Metab 2007;92:2087-99.
68. Bachrach LK, Sills IN. Clinical report-Bone densitometry in children and adolescents. Pediatrics 2011;127:189-94.
69. Seeman E, Delmas PD. Bone quality-The material and structural basis of bone strength and fragility. N Engl J Med 2006;354:2250-61.
70. Kanis JA, McClokkey EU, Johansson H, Oden A, Strom O, Borgstrom F. Development and use of FRAX in osteoporosis. Osteoporos Int 2010;21 Suppl 2:S407-13.
71. Kalra S, Kalra B, Baruah MP. Diagnosing osteoporosis made easier. FRAX tool gets better. J Med Nutr Nutr 2012;1:61-2.
72. Gogate Y, Bhadada SK. FRAX: Facts and Fantasy. Indian J Endocrinol Metab 2012;16:S224-6.
73. Gunter KB, Almstedt HC, Janz KF. Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev 2012;40:13-21.
74. Maggio AB, Rizzoli RR, Marchand LM, Ferrari S, Beghetti M, Farpour-Lambert NJ. Physical activity increases bone mineral density in children with type 1 diabetes. Med Sci Sports Exerc 2012;44:1206-11.
75. The Diabetes Control and Complications Trial Research Group. The Effect of Intensive Treatment of Diabetes on the Development and Progression of Long-Term Complications in Insulin-Dependent Diabetes Mellitus. N Engl J Med 1993;329:977-86.
76. Blazina S, Bratanic N, Campa AS, Blagus R, Orel R. Bone mineral density and importance of strict gluten-free diet in children and adolescents with celiac disease. Bone 2010;47:598-603.
77. Tau C, Mautalen C, De Rosa S, Roca A, Valenzuela X. Bone mineral density in children with celiac disease. Effect of a Gluten-free diet. Eur J Clin Nutr 2006;60:358-63.
78. Vestergaard P, Rejnmark L, Mosekilde L Are antiresorptive drugs effective against fractures in patients with diabetes? Calcif Tissue Int 2011 88 209-14.
79. Motyl KJ, McCauley LK, McCabe LR. Amelioration of type I diabetes-induced osteoporosis by parathyroid hormone is associated with improved osteoblast survival. J Cell Physiol 2012;227:1326-34.
80. Nikkel LE, Iyer SP, Mohan S, Zhang A, McMahon DJ, Tanriover B, et al.Pancreas-kidney transplantation is associated with reduced fracture risk compared with kidney-Alone transplantation in men with type 1 diabetes Kidney Int 2013;83:471-8