Diabetology International

, Volume 3, Issue 3, pp 113–130 | Cite as

Is there a link between osteoporosis and type 1 diabetes? Findings from a systematic review of the literature

  • Shaymaa Abdalwahed Abdulameer
  • Syed Azhar Syed Sulaiman
  • Mohamed Azmi Ahmad Hassali
  • Karuppiah Subramaniam
  • Mohanad Naji Sahib
Review article

Abstract

Introduction

Diabetes mellitus (DM) is a pandemic and heterogeneous metabolic disorder with significant morbidity and mortality. In addition, osteoporosis (OP) is a silent disease that constitutes an enormous socioeconomic crisis, with a harmful impact on morbidity and mortality. Therefore, this systematic review focuses on the association between OP and type 1 diabetes mellitus (T1DM).

Methods

Systematic reviews of full-length articles published in English from January 1950 to October 2010 were identified in PubMed and other available electronic databases at Universiti Sains Malaysia Library Database. The following keywords were used for the search: T1DM, insulin, OP, bone mass, and skeletal. Studies of more than 20 patients with T1DM were included.

Results

Fifty studies were identified. In general, most of the studies showed unambiguous evidence for a decrease in bone mineral density in T1DM.

Conclusions

Screening, identification and prevention of potential risk factors for OP in T1DM patients are crucial and important in terms of preserving a good quality of life in diabetic patients. Patient education about an adequate calcium and vitamin D intake and regular exercise are important for improving muscle strength and balance, and specific measures for preventing falls. Furthermore, adequate glycemic control and the prevention of diabetic complications are the starting point of therapy in T1DM.

Keywords

Bone Diabetes Osteopenia Osteoporosis Skeletal 

References

  1. 1.
    Rodbard HW, Blonde L, Braithwaite SS, Brett EM, Cobin RH, Handelsman Y, et al. American Association of Clinical Endocrinologists medical guidelines for clinical practice for the management of diabetes mellitus. Endocr Pract. 2007;13:1–68.PubMedGoogle Scholar
  2. 2.
    Roglic G, Unwin N, Bennett PH, Mathers C, Tuomilehto J, Nag S, et al. The burden of mortality attributable to diabetes. Diabetes Care. 2005;28:2130–5.PubMedCrossRefGoogle Scholar
  3. 3.
    Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047–53.PubMedCrossRefGoogle Scholar
  4. 4.
    Hadjidakis D, Mylonakis A, Sfakianakis M, Raptis A, Raptis S. Diabetes and premature menopause: is their co-existence detrimental to the skeleton? Eur J Endocrinol. 2005;152:437–42.PubMedCrossRefGoogle Scholar
  5. 5.
    Reyes B, Moreno O. Prevalence of osteopenia and osteoporosis in postmenopausal women. Aten Primaria. 2005;35:342–7.CrossRefGoogle Scholar
  6. 6.
    Cooper C, Melton L III. Epidemiology of osteoporosis. Trends Endocrinol Metab. 1992;3:224–9.PubMedCrossRefGoogle Scholar
  7. 7.
    New S. Bone health: the role of micronutrients. Br Med Bull. 1999;55:619–33.PubMedCrossRefGoogle Scholar
  8. 8.
    Lindsay R. The burden of osteoporosis: cost. Am J Med. 1995;98:9S–11S.PubMedCrossRefGoogle Scholar
  9. 9.
    Ray N, Chan J, Thamer M, Melton L III. Medical expenditures for the treatment of osteoporotic fractures in the United States in 1995: report from the National Osteoporosis Foundation. J Bone Miner Res. 1997;12:24–35.PubMedCrossRefGoogle Scholar
  10. 10.
    Gold D, Shipp K, Lyles K. Managing patients with complications of osteoporosis. Endocrin Metab Clin. 1998;27:485–96.CrossRefGoogle Scholar
  11. 11.
    Lips P, Cooper C, Agnusdei D, Caulin F, Egger P, Johnell O, et al. Quality of life in patients with vertebral fractures: validation of the quality of life questionnaire of the European Foundation for Osteoporosis (QUALEFFO). Osteoporos Int. 1999;10:150–60.PubMedCrossRefGoogle Scholar
  12. 12.
    Wolf R, Stone K, Cauley J. Update on the epidemiology of osteoporosis. Curr Rheumatol Rep. 2000;2:74–86.PubMedCrossRefGoogle Scholar
  13. 13.
    Boyle J, Honeycutt A, Narayan K, Hoerger T, Geiss L, Chen H, et al. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care. 2001;24:1936–40.PubMedCrossRefGoogle Scholar
  14. 14.
    Reid I, Evans M, Cooper G, Ames RW, Stapleton J. Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physiol Endocrinol Metab. 1993;265:E655–9.Google Scholar
  15. 15.
    Paul R, Bailey A. Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol. 1996;28:1297–310.PubMedCrossRefGoogle Scholar
  16. 16.
    Yamagishi S, Nakamura K, Inoue H. Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Med Hypotheses. 2005;65:1013–5.PubMedCrossRefGoogle Scholar
  17. 17.
    Alikhani M, Alikhani Z, Boyd C, MacLellan CM, Raptis M, Liu R, et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone. 2007;40:345–53.PubMedCrossRefGoogle Scholar
  18. 18.
    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.PubMedCrossRefGoogle Scholar
  19. 19.
    Raskin P, Stevenson MRM, Barilla DE, Pak CYC. The hypercalciuria of diabetes mellitus: its amelioration with insulin. Clin Endocrinol (Oxf). 1978;9:329–35.CrossRefGoogle Scholar
  20. 20.
    Wientroub S, Eisenberg D, Tardiman R, Weissman S, Salama R. Is diabetic osteoporosis due to microangiopathy? Lancet. 1980;2:983.PubMedCrossRefGoogle Scholar
  21. 21.
    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.PubMedCrossRefGoogle Scholar
  22. 22.
    Bonjour J, Chevalley T, Rizzoli R, Ferrari S. Gene-environment interactions in the skeletal response to nutrition and exercise during growth. Med Sport Sci. 2007;51:64–80.PubMedCrossRefGoogle Scholar
  23. 23.
    Henry Y, Fatayerji D, Eastell R. Attainment of peak bone mass at the lumbar spine, femoral neck and radius in men and women: relative contributions of bone size and volumetric bone mineral density. Osteoporos Int. 2004;15:263–73.PubMedCrossRefGoogle Scholar
  24. 24.
    Weaver C. The role of nutrition on optimizing peak bone mass. Asia Pac J Clin Nutr. 2008;17:135–7.PubMedGoogle Scholar
  25. 25.
    Genant HK, Cooper C, Poor G, Reid I, Ehrlich G, Kanis J, et al. Interim report and recommendations of the World Health Organization task-force for osteoporosis. Osteoporos Int. 1999;10:259–64.PubMedCrossRefGoogle Scholar
  26. 26.
    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.PubMedCrossRefGoogle Scholar
  27. 27.
    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. 1998;11:413–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Ersoy B, Gök en D, Darcan S, Mavi E, Öztürk C. Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr. 1999;66:375–9.PubMedCrossRefGoogle Scholar
  29. 29.
    Hough F. Alterations of bone and mineral metabolism in diabetes mellitus. II. Clinical studies in 206 patients with type I diabetes mellitus. S Afr Med J. 1987;72:120–6.PubMedGoogle Scholar
  30. 30.
    Leon M, Larrodera L, Lledo G, Hawkins F. Study of bone loss in diabetes mellitus type 1. Diabetes Res Clin Pract. 1989;6:237–42.PubMedCrossRefGoogle Scholar
  31. 31.
    Wiske P, Wentworth S, Norton J Jr, Epstein S, Johnston C Jr. Evaluation of bone mass and growth in young diabetics. Metabolism. 1982;31:848–54.PubMedCrossRefGoogle Scholar
  32. 32.
    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.PubMedCrossRefGoogle Scholar
  33. 33.
    Forst T, Beyer J, Pfützner A, Kann P, Schehler B, Lobmann R, et al. Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med. 1995;12:874–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Nevitt M, Johnell O, Black D, Ensrud K, Genant H, Cummings S. Bone mineral density predicts non-spine fractures in very elderly women. Osteoporos Int. 1994;4:325–31.PubMedCrossRefGoogle Scholar
  35. 35.
    Melton L III, Atkinson E, O’Fallon W, Wahner H, Riggs B. Long-term fracture prediction by bone mineral assessed at different skeletal sites. J Bone Miner Res. 1993;8:1227–33.PubMedCrossRefGoogle Scholar
  36. 36.
    Campos Pastor M, Lopez-Ibarra P, Escobar-Jimenez F, Serrano Pardo M, Garcia-Cervigon A. Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int. 2000;11:455–9.PubMedCrossRefGoogle Scholar
  37. 37.
    Nicodemus K, Folsom A. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24:1192–7.PubMedCrossRefGoogle Scholar
  38. 38.
    Tuominen J, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22:1196–200.PubMedCrossRefGoogle Scholar
  39. 39.
    McCarty M. Anabolic effects of insulin on bone suggest a role for chromium picolinate in preservation of bone density. Med Hypotheses. 1995;45:241–6.PubMedCrossRefGoogle Scholar
  40. 40.
    Kemink S, Hermus A, Swinkels L, Lutterman J, Smals A. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Investig. 2000;23:295–303.Google Scholar
  41. 41.
    Dixit PK, Ekstrom RA. Decreased breaking strength of diabetic rat bone and its improvement by insulin treatment. Calcif Tissue Int. 1980;32:195–9.PubMedCrossRefGoogle Scholar
  42. 42.
    Bennet W, Connacher A, Jung R, Stehle P, Rennie M. Effects of insulin and amino acids on leg protein turnover in IDDM patients. Diabetes. 1991;40:499–508.PubMedCrossRefGoogle Scholar
  43. 43.
    Pacy P, Bannister P, Halliday D. Influence of insulin on leucine kinetics in the whole body and across the forearm in post-absorptive insulin dependent diabetic (type 1) patients. Diabetes Res. 1991;18:155–62.PubMedGoogle Scholar
  44. 44.
    López-Ibarra PJ, Pastor MMC, Escobar-Jiménez F, Pardo MDS, González AG, Luna JDD, et al. Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract. 2001;7:346–51.PubMedGoogle Scholar
  45. 45.
    Bonfanti R, Mora S, Prinster C, Bognetti E, Meschi F, Puzzovio M, 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.PubMedCrossRefGoogle Scholar
  46. 46.
    De Schepper J, Smitz J, Rosseneu S, Bollen P, Louis O. Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res Paediatr. 1998;50:193–6.Google Scholar
  47. 47.
    McNair P, Christiansen C, Christensen M, Madsbad S, Faber O, Binder C, et al. Development of bone mineral loss in insulin-treated diabetes: a 1 1/2 years follow-up study in sixty patients. Eur J Clin Investig. 1981;11:55–9.CrossRefGoogle Scholar
  48. 48.
    Rosenbloom A, Lezotte D, Weber F, Gudat J, Heller D, Weber M, et al. Diminution of bone mass in childhood diabetes. Diabetes. 1977;26:1052–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Izaolaa M, Escuderoe E, Herrerose V. Effects of dietary intake and life style on bone density in patients with diabetes mellitus type 2. Ann Nutr Metab. 2004;48:141–5.CrossRefGoogle Scholar
  50. 50.
    Deutschmann H, Weger M, Weger W, Kotanko P, Deutschmann M, Skrabal F. Search for occult secondary osteoporosis: impact of identified possible risk factors on bone mineral density. J Intern Med. 2002;252:389–97.PubMedCrossRefGoogle Scholar
  51. 51.
    Inzerillo A, Epstein S. Osteoporosis and diabetes mellitus. Rev Endocr Metab Disord. 2004;5:261–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Olmos J, Perez-Castrillon J, Garcia M, Garrido J, Amado J, Gonzalez-Macias J. Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner. 1994;26:1–8.PubMedCrossRefGoogle Scholar
  53. 53.
    Morrison L, Bogan I. Bone development in diabetic children: a roentgen study. Am J Med Sci. 1927;174:313–8.CrossRefGoogle Scholar
  54. 54.
    Albright F, Reifenstein E. Bone development in diabetic children: a roentgen study. Am J Med Sci. 1948;174:313–9.Google Scholar
  55. 55.
    Menczel J, Makin M, Robin G, Jaye I, Naor E. Prevalence of diabetes mellitus in Jerusalem; its association with presenile osteoporosis. Isr J Med Sci. 1972;8:918–9.PubMedGoogle Scholar
  56. 56.
    Levin M, Boisseau V, Avioli L. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med. 1976;294:241–5.PubMedCrossRefGoogle Scholar
  57. 57.
    Leidig-Bruckner G, Ziegler R. Diabetes mellitus: a risk for osteoporosis? Exp Clin Endocrinol Diabetes. 2001;109:493–514.CrossRefGoogle Scholar
  58. 58.
    Cavanagh P, Derr J, Ulbrecht J, Maser R, Orchard T. Problems with gait and posture in neuropathic patients with insulin dependent diabetes mellitus. Diabet Med. 1992;9:469–74.PubMedCrossRefGoogle Scholar
  59. 59.
    Simoneau G, Ulbrecht J, Derr J, Becker M, Cavanagh P. Postural instability in patients with diabetic sensory neuropathy. Diabetes Care. 1994;17:1411–21.PubMedCrossRefGoogle Scholar
  60. 60.
    Alffram P. An epidemiologic study of cervical and trochanteric fractures of the femur in an urban population. Acta Orthop Scand. 1964;65:1–109.Google Scholar
  61. 61.
    Liu E, Wactawski-Wende J, Donahue R, Dmochowski J, Hovey K, Quattrin T. Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care. 2003;26:2365–9.PubMedCrossRefGoogle Scholar
  62. 62.
    Valerio G, Puente A, Buono P, Esposito A, Zanatta M, Mozzillo E, et al. Quantitative ultrasound of proximal phalanxes in patients with type 1 diabetes mellitus. Diabetes Res Clin Pract. 2004;64:161–6.PubMedCrossRefGoogle Scholar
  63. 63.
    Piepkorn B, Kann P, Forst T, Andreas J, Pfutzner A, Beyer J. Bone mineral density and bone metabolism in diabetes mellitus. Horm Metab Res. 1997;29:584–91.PubMedCrossRefGoogle Scholar
  64. 64.
    De Schepper J, Smitz J, Rosseneu S, Bollen P, Louis O. Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res. 2000;50:193–6.CrossRefGoogle Scholar
  65. 65.
    Brandao F, Vicente E, Daltro C, Sacramento M, Moreira A, Adan L. Bone metabolism is linked to disease duration and metabolic control in type 1 diabetes mellitus. Diabetes Res Clin Pract. 2007;78:334–9.PubMedCrossRefGoogle Scholar
  66. 66.
    Pascual J, Argente J, Lopez M, Munoz M, Martinez G, Vazquez M, et al. Bone mineral density in children and adolescents with diabetes mellitus type 1 of recent onset. Calcif Tissue Int. 1998;62:31–5.PubMedCrossRefGoogle Scholar
  67. 67.
    Ponder SW, McCormick DP, Daniel Fawcett H, Tran AD. Bone mineral density of the lumbar vertebrae in children and adolescents with insulin-dependent diabetes mellitus. J Pediatr. 1992;120:541–5.PubMedCrossRefGoogle Scholar
  68. 68.
    Gunczler P, Lanes R, Paoli M, Martinis R, Villaroel O, Weisinger J. Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab. 2001;14:525–8.PubMedCrossRefGoogle Scholar
  69. 69.
    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.PubMedCrossRefGoogle Scholar
  70. 70.
    Salvatoni A, Mancassola G, Biasoli R, Cardani R, Salvatore S, Broggini M, et al. Bone mineral density in diabetic children and adolescents: a follow-up study. Bone. 2004;34:900–4.PubMedCrossRefGoogle Scholar
  71. 71.
    Leger J, Marinovic D, Alberti C, Dorgeret S, Chevenne D, Marchal C, et al. Lower bone mineral content in children with type 1 diabetes mellitus is linked to female sex, low insulin-like growth factor type I levels, and high insulin requirement. J Clin Endocrinol Metab. 2006;91:3947–53.PubMedCrossRefGoogle Scholar
  72. 72.
    Bechtold S, Putzker S, Bonfig W, Fuchs O, Dirlenbach I, Schwarz H. Bone size normalizes with age in children and adolescents with type 1 diabetes. Diabetes Care. 2007;30:2046–50.PubMedCrossRefGoogle Scholar
  73. 73.
    Heap J, Murray M, Miller S, Jalili T, Moyer-Mileur L. Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr. 2004;144:56–62.PubMedCrossRefGoogle Scholar
  74. 74.
    Saha M, Sievänen H, Salo M, Tulokas S, Saha H. Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int. 2009;20:1401–6.PubMedCrossRefGoogle Scholar
  75. 75.
    Moyer-Mileur LJ, Dixon SB, Quick JL, Askew EW, Murray MA. Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr. 2004;145:662–9.PubMedCrossRefGoogle Scholar
  76. 76.
    Damilakis J, Galanakis E, Mamoulakis D, Sbyrakis S, Gourtsoyiannis N. Quantitative ultrasound measurements in children and adolescents with: type 1 diabetes. Calcif Tissue Int. 2004;74:424–8.PubMedCrossRefGoogle Scholar
  77. 77.
    D’Ercole AJ, Stiles AD, Underwood LE. Tissue concentrations of somatomedin C: further evidence for multiple sites of synthesis and paracrine or autocrine mechanisms of action. Proc Nat Acad Sci USA. 1984;81:935–9.PubMedCrossRefGoogle Scholar
  78. 78.
    Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-Ibarra P, Luna J. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int. 1996;58:316–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Hadjidakis D, Raptis A, Sfakianakis M, Mylonakis A, Raptis S. Bone mineral density of both genders in Type 1 diabetes according to bone composition. J Diabetes Complicat. 2006;20:302–7.PubMedCrossRefGoogle Scholar
  80. 80.
    Miazgowski T, Pynka S, Noworyta-Zietara M, Krzyzanowska-Swiniarska B, Pikul R. Bone mineral density and hip structural analysis in type 1 diabetic men. Eur J Endocrinol. 2007;156:123–7.PubMedCrossRefGoogle Scholar
  81. 81.
    Alexopoulou O, Jamart J, Devogelaer J, Brichard S, De Nayer P, Buysschaert M. Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabetes Metab. 2006;32:453–8.PubMedCrossRefGoogle Scholar
  82. 82.
    Hamilton E, Rakic V, Davis W, Chubb S, Kamber N, Prince R, et al. Prevalence and predictors of osteopenia and osteoporosis in adults with Type 1 diabetes. Diabet Med. 2009;26:45–52.PubMedCrossRefGoogle Scholar
  83. 83.
    Cordey J, Schneider M, Belendez C, Ziegler WJ, Rahn BA, Perren SM. Effect of bone size, not density, on the stiffness of the proximal part of normal and osteoporotic human femora. J Bone Miner Res. 1992;7:S437–44.PubMedCrossRefGoogle Scholar
  84. 84.
    Vega E, Ghiringhelli G, Mautalen C, Rey Valzacchi G, Scaglia H, Zylberstein C. Bone mineral density and bone size in men with primary osteoporosis and vertebral fractures. Calcif Tissue Int. 1998;62:465–9.PubMedCrossRefGoogle Scholar
  85. 85.
    Deng HW, Xu FH, Davies KM, Heaney R, Recker RR. Differences in bone mineral density, bone mineral content, and bone areal size in fracturing and non-fracturing women, and their interrelationships at the spine and hip. J Bone Miner Metab. 2002;20:358–66.PubMedCrossRefGoogle Scholar
  86. 86.
    Seeman E. The structural basis of bone fragility in men. Bone. 1999;25:143–7.PubMedCrossRefGoogle Scholar
  87. 87.
    Cummings SR, Kelsey JL, Nevitt MC, O’Dowd KJ. Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev. 1985;7:178–208.PubMedGoogle Scholar
  88. 88.
    McNair P, Madsbad S, Christiansen C, Faber O, Transbøl I, Binder C. Osteopenia in insulin treated diabetes mellitus. Diabetologia. 1978;15:87–90.PubMedCrossRefGoogle Scholar
  89. 89.
    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.PubMedCrossRefGoogle Scholar
  90. 90.
    Kayath M, Tavares E, Dib S, Vieira J. Prospective bone mineral density evaluation in patients with insulin-dependent diabetes mellitus. J Diabetes Complicat. 1998;12:133–9.PubMedCrossRefGoogle Scholar
  91. 91.
    Ingberg C, Palmer M, Åman J, Arvidsson B, Schvarcz E, Berne C. Body composition and bone mineral density in long standing type 1 diabetes. J Intern Med. 2004;255:392–8.PubMedCrossRefGoogle Scholar
  92. 92.
    Bridges M, Moochhala S, Barbour J, Kelly C. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol. 2005;42:82–6.PubMedCrossRefGoogle Scholar
  93. 93.
    Compston J, Smith E, Matthews C, Schofield P. Whole body composition and regional bone mass in women with insulin dependent diabetes mellitus. Clin Endocrinol (Oxf). 1994;41:289–93.CrossRefGoogle Scholar
  94. 94.
    Bouillon R. Diabetic bone disease. Calcif Tissue Int. 1991;49:155–60.PubMedCrossRefGoogle Scholar
  95. 95.
    Mastrandrea L, Wactawski-Wende J, Donahue R, Hovey K, 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.PubMedCrossRefGoogle Scholar
  96. 96.
    Strotmeyer E, Cauley J, Orchard T, Steenkiste A, Dorman J. 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.PubMedCrossRefGoogle Scholar
  97. 97.
    Hampson G, Evans C, Petitt R, Evans W, Woodhead S, Peters J, et al. Bone mineral density, collagen type 1 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia. 1998;41:1314–20.PubMedCrossRefGoogle Scholar
  98. 98.
    Forsen L, Meyer H, Midthjell K, Edna T. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trøndelag Health Survey. Diabetologia. 1999;42:920–5.PubMedCrossRefGoogle Scholar
  99. 99.
    Buysschaert M, Cauwe F, Jamart J, Brichant C, De Coster P, Magnan A, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabetes Metab. 1992;18:32–7.Google Scholar
  100. 100.
    Lunt H, Florkowski C, Cundy T, Kendall D, Brown L, Elliot J, 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.PubMedCrossRefGoogle Scholar
  101. 101.
    Cummings S, Bates D, Black D. Clinical use of bone densitometry: scientific review. JAMA. 2002;288:1889–97.PubMedCrossRefGoogle Scholar
  102. 102.
    Ross PD, Davis JW, Epstein RS, Wasnich RD. Pre-existing fractures and bone mass predict vertebral fracture incidence in women. Ann Intern Med. 1991;114:919–23.PubMedGoogle Scholar
  103. 103.
    Black DM, Arden NK, Palermo L, Pearson J, Cummings SR. Prevalent vertebral deformities predict hip fractures and new vertebral deformities but not wrist fractures. J Bone Miner Res. 1999;14:821–8.PubMedCrossRefGoogle Scholar
  104. 104.
    Klotzbuecher CM, Ross PD, Landsman PB, Abbott TA III, Berger M. Patients with prior fractures have an increased risk of future fractures: a summary of the literature and statistical synthesis. J Bone Miner Res. 2000;15:721–39.PubMedCrossRefGoogle Scholar
  105. 105.
    Burger H, De Laet C, Weel A, Hofman A, Pols H. Added value of bone mineral density in hip fracture risk scores. Bone. 1999;25:369–74.PubMedCrossRefGoogle Scholar
  106. 106.
    Fowkes F. Aetiology of peripheral atherosclerosis. Br Med J. 1989;298:405.CrossRefGoogle Scholar
  107. 107.
    Slemenda CW, Hui SL, Longcope C, Johnston CC Jr. Cigarette smoking, obesity, and bone mass. J Bone Miner Res. 1989;4:737–41.PubMedCrossRefGoogle Scholar
  108. 108.
    Ortego-Centeno N, Muñoz-Torres M, Hernandez-Quero J, Jurado-Duce A, Higuera Torres-Puchol J. Bone mineral density, sex steroids, and mineral metabolism in premenopausal smokers. Calcif Tissue Int. 1994;55:403–7.PubMedCrossRefGoogle Scholar
  109. 109.
    Nuti R, Martini G. Measurements of bone mineral density by DXA total body absorptiometry in different skeletal sites in postmenopausal osteoporosis. Bone. 1992;13:173–8.PubMedCrossRefGoogle Scholar
  110. 110.
    Staa TP, Leufkens H, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int. 2002;13:777–87.PubMedCrossRefGoogle Scholar
  111. 111.
    Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE, et al. Risk factors for hip fracture in white women. N Engl J Med. 1995;332:767–74.PubMedCrossRefGoogle Scholar
  112. 112.
    Dargent-Molina P, Schott A, Hans D, Favier F, Grandjean H, Baudoin C, et al. Separate and combined value of bone mass and gait speed measurements in screening for hip fracture risk: results from the EPIDOS study. Osteoporos Int. 1999;9:188–92.PubMedCrossRefGoogle Scholar
  113. 113.
    Garnero P, Hausherr E, Chapuy MC, Marcelli C, Grandjean H, Muller C, et al. Markers of bone resorption predict hip fracture in elderly women: the EPIDOS Prospective Study. J Bone Miner Res. 1996;11:1531–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Cummings SR, Browner WS, Bauer D, Stone K, Ensrud K, Jamal S, et al. Endogenous hormones and the risk of hip and vertebral fractures among older women. N Engl J Med. 1998;339:733–8.PubMedCrossRefGoogle Scholar
  115. 115.
    Peechakara SV, Pittas AG. Vitamin D as a potential modifier of diabetes risk. Nat Clin Pract Endocrinol Metab. 2008;4:182–3.PubMedCrossRefGoogle Scholar
  116. 116.
    Danescu LG, Levy S, Levy J. Vitamin D and diabetes mellitus. Endocrine. 2009;35:11–7.PubMedCrossRefGoogle Scholar
  117. 117.
    Holick MF. The vitamin D epidemic and its health consequences. J Nutr. 2005;135:2739S–48S.PubMedGoogle Scholar
  118. 118.
    Hamann C, Kirschner S, Günther KP, Hofbauer LC. Bone, sweet bone—osteoporotic fractures in diabetes mellitus. Nat Rev Endocrinol. 2012;8:297–305.PubMedCrossRefGoogle Scholar
  119. 119.
    Rozadilla A, Nolla J, Montana E, Fiter J, Gomez-Vaquero C, Soler J, et al. Bone mineral density in patients with type 1 diabetes mellitus. Jt Bone Spine. 2000;67:215–8.Google Scholar
  120. 120.
    Clausen P, Feldt-Rasmussen B, Jacobsen P, Rossing K, Parving H, Nielsen P, et al. Microalbuminuria as an early indicator of osteopenia in male insulin-dependent diabetic patients. Diabet Med. 1997;14:1038–43.PubMedCrossRefGoogle Scholar
  121. 121.
    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.PubMedCrossRefGoogle Scholar
  122. 122.
    Singer DE, Nathan DM, Fogel HA, Schachat AP. Screening for diabetic retinopathy. Ann Intern Med. 1992;116:660–71.PubMedGoogle Scholar
  123. 123.
    Brown SA, Sharpless JL. Osteoporosis: an under-appreciated complication of diabetes. Clin Diabetes. 2004;22:10–20.CrossRefGoogle Scholar
  124. 124.
    Manaviat M, Afkhami M, Shoja M. Retinopathy and microalbuminuria in type II diabetic patients. BMC Ophthalmol. 2004;4:9.PubMedCrossRefGoogle Scholar
  125. 125.
    Ivers R, Cumming R, Mitchell P, Peduto A. Diabetes and risk of fracture. Diabetes Care. 2001;24:1198–203.PubMedCrossRefGoogle Scholar
  126. 126.
    Mathiassen B, Nielsen S, Johansen JS, Hartwell D, Ditzel J, Rødbro P, et al. Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. J Diabetes Complicat. 1990;4:145–9.CrossRefGoogle Scholar
  127. 127.
    Sahib MN, Abdulameer SA, Aziz NA, Hassan Y. Pathogenesis of diabetic kidney disease: review of cellular aspects of renal lesions. Afr J Pharm Pharacol. 2009;3:507–14.Google Scholar
  128. 128.
    Epstein FH, Hruska KA, Teitelbaum SL. Renal osteodystrophy. N Engl J Med. 1995;333:166–75.CrossRefGoogle Scholar
  129. 129.
    Kaji H, Suzuki M, Yano S, Sugimoto T, Chihara K, Hattori S, et al. Risk factors for hip fracture in hemodialysis patients. Am J Nephrol. 2000;22:325–31.CrossRefGoogle Scholar
  130. 130.
    Nishitani H, Miki T, Morii H, Nishizawa Y, Ishimura E, Hagiwara S, et al. Decreased bone mineral density in diabetic patients on hemodialysis. Contrib Nephrol. 1991;90:223–7.PubMedGoogle Scholar
  131. 131.
    Hercz G, Sherrard D, Chan W, Pei Y. Aplastic osteodystrophy: follow-up after 5 years. J Am Soc Nephrol. 1994;5:851.Google Scholar
  132. 132.
    Garraway W, Stauffer R, Kurland L, O’Fallon W. Limb fractures in a defined population. I. Frequency and distribution. Mayo Clin Proc. 1979;54:701–7.PubMedGoogle Scholar
  133. 133.
    Masud T, Langley S, Wiltshire P, Doyle D, Spector T. Effect of spinal osteophytosis on bone mineral density measurements in vertebral osteoporosis. Br Med J. 1993;307:172–3.CrossRefGoogle Scholar
  134. 134.
    Weber TJ, Quarles LD. Preventing bone loss after renal transplantation with bisphosphonates: We can…but should we? Kidney Int. 2000;57:735–7.PubMedCrossRefGoogle Scholar
  135. 135.
    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. 2007;24:91–3.PubMedCrossRefGoogle Scholar
  136. 136.
    Boulton A. Late sequelae of diabetic neuropathy. Diabetic neuropathy. 1997; 63–76.Google Scholar
  137. 137.
    Boulton A, Gries F, Jervell J. Guidelines for the diagnosis and outpatient management of diabetic peripheral neuropathy. Diabet Med. 1998;15:508–14.PubMedCrossRefGoogle Scholar
  138. 138.
    Aronson J. Temporal and spatial increases in blood flow during distraction osteogenesis. Clin Orthop. 1994;301:124–31.PubMedGoogle Scholar
  139. 139.
    Young MJ, Marshall A, Adams JE, Selby PL, Boulton AJM. Osteopenia, neurological dysfunction, and the development of Charcot neuroarthropathy. Diabetes Care. 1995;18:34–8.PubMedCrossRefGoogle Scholar
  140. 140.
    Gundersen HJG. Peripheral blood flow and metabolic control in juvenile diabetes. Diabetologia. 1974;10:225–31.PubMedCrossRefGoogle Scholar
  141. 141.
    Maser RE, Wolfson S, Ellis D, Stein EA, Drash AL, Becker DJ, et al. Cardiovascular disease and arterial calcification in insulin-dependent diabetes mellitus: interrelations and risk factor profiles. Pittsburgh Epidemiology of Diabetes Complications Study-V. Arterioscler Thromb Vasc Biol. 1991;11:958–65.CrossRefGoogle Scholar
  142. 142.
    Osmundson PJ, O’Fallon WM, Zimmerman BR, Kazmier FJ, Langworthy AL, Palumbo P. Course of peripheral occlusive arterial disease in diabetes. Vascular laboratory assessment. Diabetes Care. 1990;13:143–52.PubMedCrossRefGoogle Scholar
  143. 143.
    Fasching P, Kurzemann S, Wagner B, Wagner O, Waldhäusl W, Ehringer H, et al. Only marginal influence of metabolic control on blood rheology in insulin-dependent diabetic patients without manifest angiopathy. Clin Hemorheol. 1995;15:3–11.Google Scholar
  144. 144.
    Vigilance JE, Reid HL. Glycaemic control influences peripheral blood flow and haemorheological variables in patients with diabetes mellitus. Clin Hemorheol Microcirc. 2005;33:337–46.PubMedGoogle Scholar
  145. 145.
    Wallace C, Reiber GE, LeMaster J, Smith DG, Sullivan K, Hayes S, et al. Incidence of falls, risk factors for falls, and fall-related fractures in individuals with diabetes and a prior foot ulcer. Diabetes Care. 2002;25:1983–6.PubMedCrossRefGoogle Scholar
  146. 146.
    Frost H. Wolff’s Law and bone’s structural adaptations to mechanical usage: an overview for clinicians. Angle Orthod. 1994;64:175–88.PubMedGoogle Scholar
  147. 147.
    Qin YX, Rubin CT, McLeod KJ. Nonlinear dependence of loading intensity and cycle number in the maintenance of bone mass and morphology. J Orthop Res. 1998;16:482–9.PubMedCrossRefGoogle Scholar
  148. 148.
    Wallace B, Cumming R. Systematic review of randomized trials of the effect of exercise on bone mass in pre-and postmenopausal women. Calcif Tissue Int. 2000;67:10–8.PubMedCrossRefGoogle Scholar
  149. 149.
    Bonaiuti D, Shea B, Iovine R, Negrini S, Robinson V, Kemper H, et al. Exercise for preventing and treating osteoporosis in postmenopausal women. Cochrane Database Syst Rev. 2002;3:CD000333.Google Scholar
  150. 150.
    Yamazaki S, Ichimura S, Iwamoto J, Takeda T, Toyama Y. Effect of walking exercise on bone metabolism in postmenopausal women with osteopenia/osteoporosis. J Bone Miner Metab. 2004;22:500–8.PubMedCrossRefGoogle Scholar
  151. 151.
    Wongdee K, Charoenphandhu N. Osteoporosis in diabetes mellitus: possible cellular and molecular mechanisms. World J Diabetes. 2011;2:41–8.PubMedCrossRefGoogle Scholar
  152. 152.
    Warburton DER, Gledhill N, Quinney A. The effects of changes in musculoskeletal fitness on health. Can J Appl Physiol. 2001;26:161–216.PubMedCrossRefGoogle Scholar
  153. 153.
    Wolff I, Van Croonenborg J, Kemper H, Kostense P, Twisk J. The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre-and postmenopausal women. Osteoporos Int. 1999;9:1–12.PubMedCrossRefGoogle Scholar
  154. 154.
    Tinetti ME, Baker DI, McAvay G, Claus EB, Garrett P, Gottschalk M, et al. A multifactorial intervention to reduce the risk of falling among elderly people living in the community. N Engl J Med. 1994;331:821–7.PubMedCrossRefGoogle Scholar
  155. 155.
    Shaw JM, Snow CM. Weighted vest exercise improves indices of fall risk in older women. J Gerontol A Biol Sci Med Sci. 1998;53:M53–8.PubMedCrossRefGoogle Scholar
  156. 156.
    Bevier WC, Wiswell RA, Pyka G, Kozak KC, Newhall KM, Marcus R. Relationship of body composition, muscle strength, and aerobic capacity to bone mineral density in older men and women. J Bone Miner Res. 1989;4:421–32.PubMedCrossRefGoogle Scholar
  157. 157.
    Lindsey C, Brownbill RA, Bohannon RA, Ilich JZ. Association of physical performance measures with bone mineral density in postmenopausal women. Arch Phys Med Rehabil. 2005;86:1102–7.PubMedCrossRefGoogle Scholar
  158. 158.
    Khazzani H, Allali F, Bennani L, Ichchou L, El Mansouri L, Abourazzak F, et al. The relationship between physical performance measures, bone mineral density, falls, and the risk of peripheral fracture: a cross-sectional analysis. BMC Public Health. 2009;9:297.PubMedCrossRefGoogle Scholar
  159. 159.
    Shore RM, Chesney RW, Mazess RB, Rose PG, Bargman GJ. Osteopenia in juvenile diabetes. Calcif Tissue Int. 1981;33:455–7.PubMedCrossRefGoogle Scholar
  160. 160.
    Weber G, Beccaria L, de’Angelis M, Mora S, Galli L, Cazzuffi M, et al. Bone mass in young patients with type I diabetes. Bone Miner. 1990;8:23–30.PubMedCrossRefGoogle Scholar
  161. 161.
    Roe TF, Mora S, Costin G, Kaufman F, Carlson ME, Gilsanz V. Vertebral bone density in insulin-dependent diabetic children. Metabolism. 1991;40:967–71.PubMedCrossRefGoogle Scholar
  162. 162.
    Camurdan MO, Ciaz P, Bideci A, Demirel F. Role of hemoglobin A1c, duration and puberty on bone mineral density in diabetic children. Pediatr Int. 2007;49:645–51.PubMedCrossRefGoogle Scholar
  163. 163.
    Krakauer J, McKenna M, Buderer N, Rao D, Whitehouse F, Parfitt A. Bone loss and bone turnover in diabetes. Diabetes. 1995;44:775–82.PubMedCrossRefGoogle Scholar

Copyright information

© The Japan Diabetes Society 2012

Authors and Affiliations

  • Shaymaa Abdalwahed Abdulameer
    • 1
  • Syed Azhar Syed Sulaiman
    • 1
  • Mohamed Azmi Ahmad Hassali
    • 1
  • Karuppiah Subramaniam
    • 2
  • Mohanad Naji Sahib
    • 1
  1. 1.School of Pharmaceutical SciencesUniversiti Sains MalaysiaMindenMalaysia
  2. 2.Diabetes Out Patient ClinicPenang General HospitalPenangMalaysia

Personalised recommendations