Skip to main content
Top
Published in: Osteoporosis International 4/2007

01-04-2007 | Original Article

Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis

Author: P. Vestergaard

Published in: Osteoporosis International | Issue 4/2007

Login to get access

Abstract

Introduction and hypothesis

Diabetes affects bone metabolism. The hypothesis was that type 1 (T1D) and type 2 (T2D) affects BMD and fracture risk differently.

Material and methods

Pubmed, Embase, and Web of Science were searched using the terms “diabetes”, “fracture”, and “bone mineral”.

Results

Hip fracture risk was increased in T1D (RR = 6.94, 95% CI: 3.25–14.78, five studies) and T2D (1.38, 95% CI: 1.25–1.53, eight studies) compared to subjects without diabetes. The increase in relative hip fracture risk was significantly higher in T1D than in T2D. BMD Z-score was decreased in the spine (mean ± SEM −0.22 ± 0.01) and hip (−0.37 ± 0.16) in T1D and increased in the spine (0.41 ± 0.01) and hip (0.27 ± 0.01) in T2D. A meta-regression showed that body mass index (BMI) was a major determinant for BMD in both the spine and hip. Glycated haemoglobin (HbA1C) was not linked to BMD. The increase in fracture risk was higher and BMD lower in patients with complications to diabetes.

Conclusions

Hip fracture risk is increased in both T1D and T2D, whereas BMD is increased in T2D and decreased in T1D. A common factor such as complications may explain the increase in fracture risk, whereas BMI may ameliorate the increase in fracture risk in T2D.
Literature
1.
go back to reference McNair P, Madsbad S, Christensen MS et al (1979) Bone mineral loss in insulin-treated diabetes mellitus: studies on pathogenesis. Acta Endocrinol 90:463–472PubMed McNair P, Madsbad S, Christensen MS et al (1979) Bone mineral loss in insulin-treated diabetes mellitus: studies on pathogenesis. Acta Endocrinol 90:463–472PubMed
2.
go back to reference McNair P, Christiansen C, Christensen MS et al (1981) Development of bone mineral loss in insulin-treated diabetes: a 1 1/2 years follow-up study in sixty patients. European Journal of Clinical Investigation 11:55–59PubMed McNair P, Christiansen C, Christensen MS et al (1981) Development of bone mineral loss in insulin-treated diabetes: a 1 1/2 years follow-up study in sixty patients. European Journal of Clinical Investigation 11:55–59PubMed
3.
go back to reference Forsen L, Meyer HE, Midthjell K et al (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42:920–925PubMed Forsen L, Meyer HE, Midthjell K et al (1999) Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia 42:920–925PubMed
4.
go back to reference Raskin P, Stevenson MRM, Barilla DE et al (1978) The hypercalciuria of diabetes mellitus: its amelioration with insulin. Clin Endocrinol 9:329–335 Raskin P, Stevenson MRM, Barilla DE et al (1978) The hypercalciuria of diabetes mellitus: its amelioration with insulin. Clin Endocrinol 9:329–335
5.
go back to reference McNair P, Christensen MS, Madsbad S et al (1981) Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 96:81–86 McNair P, Christensen MS, Madsbad S et al (1981) Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 96:81–86
6.
go back to reference Bouillon R (1991) Diabetic bone disease [editorial]. Calcif Tissue Int 49:155–160PubMed Bouillon R (1991) Diabetic bone disease [editorial]. Calcif Tissue Int 49:155–160PubMed
7.
go back to reference Jehle PM, Jehle DR, Mohan S et al (1998) 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 159:297–306PubMed Jehle PM, Jehle DR, Mohan S et al (1998) 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 159:297–306PubMed
8.
go back to reference Hein G, Wiegand R, Lehmann G et al (2003) Advanced glycation end-products pentosidine and N epsilon-carboxymethyllysine are elevated in serum of patients with osteoporosis. Rheumatology (Oxford) 42:1242–1246 Hein G, Wiegand R, Lehmann G et al (2003) Advanced glycation end-products pentosidine and N epsilon-carboxymethyllysine are elevated in serum of patients with osteoporosis. Rheumatology (Oxford) 42:1242–1246
9.
go back to reference Hein G, Weiss C, Lehmann G et al (2006) Advanced glycation end product modification of bone proteins and bone remodelling: hypothesis and preliminary immunohistochemical findings. Ann Rheum Dis 65:101–104PubMed Hein G, Weiss C, Lehmann G et al (2006) Advanced glycation end product modification of bone proteins and bone remodelling: hypothesis and preliminary immunohistochemical findings. Ann Rheum Dis 65:101–104PubMed
10.
go back to reference Miyata T, Notoya K, Yoshida K et al (1997) 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 8:260–270PubMed Miyata T, Notoya K, Yoshida K et al (1997) 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 8:260–270PubMed
11.
go back to reference Miyata T, Kawai R, Taketomi S et al (1996) Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant 11(Suppl 5):54–57PubMed Miyata T, Kawai R, Taketomi S et al (1996) Possible involvement of advanced glycation end-products in bone resorption. Nephrol Dial Transplant 11(Suppl 5):54–57PubMed
12.
go back to reference Odetti P, Rossi S, Monacelli F et al (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717PubMed Odetti P, Rossi S, Monacelli F et al (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717PubMed
13.
go back to reference Saito M, Fujii K, Soshi S et al (2006) Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos Int Saito M, Fujii K, Soshi S et al (2006) Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos Int
14.
go back to reference Yamagishi S, Nakamura K, Inoue H (2005) Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Medical Hypotheses 65:1013–1015PubMed Yamagishi S, Nakamura K, Inoue H (2005) Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Medical Hypotheses 65:1013–1015PubMed
15.
go back to reference Cozen L (1972) Does diabetes delay fracture healing? Clin Orthop 82:134–140PubMed Cozen L (1972) Does diabetes delay fracture healing? Clin Orthop 82:134–140PubMed
16.
go back to reference Inaba M, Okuno S, Kumeda Y et al (2005) Increased incidence of vertebral fracture in older female hemodialyzed patients with type 2 diabetes mellitus. Calcif Tissue Int 76:256–260PubMed Inaba M, Okuno S, Kumeda Y et al (2005) Increased incidence of vertebral fracture in older female hemodialyzed patients with type 2 diabetes mellitus. Calcif Tissue Int 76:256–260PubMed
17.
go back to reference Nisbeth U, Lindh E, Ljunghall S et al (1999) Increased fracture rate in diabetes mellitus and females after renal transplantation. Transplantation 67:1218–1222PubMed Nisbeth U, Lindh E, Ljunghall S et al (1999) Increased fracture rate in diabetes mellitus and females after renal transplantation. Transplantation 67:1218–1222PubMed
18.
go back to reference Rix M, Andreassen H, Eskildsen P (1999) Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22:827–831PubMed Rix M, Andreassen H, Eskildsen P (1999) Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22:827–831PubMed
19.
go back to reference McNair P, Christensen MS, Christiansen C et al (1981) Is diabetic osteoporosis due to microangiopathy? Lancet 1:1271PubMed McNair P, Christensen MS, Christiansen C et al (1981) Is diabetic osteoporosis due to microangiopathy? Lancet 1:1271PubMed
20.
go back to reference Vogt MT, Cauley JA, Kuller LH et al (1997) Bone mineral density and blood flow to the lower extremities: the study of osteoporotic fractures. J Bone Miner Res 12:283–289PubMed Vogt MT, Cauley JA, Kuller LH et al (1997) Bone mineral density and blood flow to the lower extremities: the study of osteoporotic fractures. J Bone Miner Res 12:283–289PubMed
21.
go back to reference Hadjidakis D, Diamantopoulos E, Kokkinakis E, Sfakianakis M, Merakos G, Raptis SA (1997) Bone mineral density in type II diabetics with macroangiopathy. J Bone Miner Res 12(Suppl 1):S516 Hadjidakis D, Diamantopoulos E, Kokkinakis E, Sfakianakis M, Merakos G, Raptis SA (1997) Bone mineral density in type II diabetics with macroangiopathy. J Bone Miner Res 12(Suppl 1):S516
22.
go back to reference Maurer MS, Burcham J, Cheng H (2005) 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 60:1157–1162PubMed Maurer MS, Burcham J, Cheng H (2005) 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 60:1157–1162PubMed
23.
go back to reference Kennedy RL, Henry J, Chapman AJ et al (2002) Accidents in patients with insulin-treated diabetes: increased risk of low-impact falls but not motor vehicle crashes-a prospective register-based study. J Trauma 52:660–666PubMed Kennedy RL, Henry J, Chapman AJ et al (2002) Accidents in patients with insulin-treated diabetes: increased risk of low-impact falls but not motor vehicle crashes-a prospective register-based study. J Trauma 52:660–666PubMed
24.
go back to reference Nabarro JD (1985) Compression fractures of the dorsal spine in hypoglycaemic fits in diabetes. Br Med J (Clin Res Ed) 291:1320CrossRef Nabarro JD (1985) Compression fractures of the dorsal spine in hypoglycaemic fits in diabetes. Br Med J (Clin Res Ed) 291:1320CrossRef
25.
go back to reference Pal B (1985) Compression fractures of the dorsal spine in hypoglycemic fits in diabetes. Br Med J (Clin Res Ed) 291:1646 Pal B (1985) Compression fractures of the dorsal spine in hypoglycemic fits in diabetes. Br Med J (Clin Res Ed) 291:1646
26.
go back to reference Tuominen JT, Impivaara O, Puukka P et al (1999) Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200PubMed Tuominen JT, Impivaara O, Puukka P et al (1999) Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200PubMed
27.
go back to reference van Daele PL, Stolk RP, Burger H et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med 122:409–414PubMed van Daele PL, Stolk RP, Burger H et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med 122:409–414PubMed
28.
go back to reference Heath III H, Melton III LJ, Chu CP (1980) Diabetes mellitus and risk of skeletal fracture. N Engl J Med 303:567–570PubMedCrossRef Heath III H, Melton III LJ, Chu CP (1980) Diabetes mellitus and risk of skeletal fracture. N Engl J Med 303:567–570PubMedCrossRef
29.
go back to reference de Liefde II, van der KM, de Laet CE et al (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporosis Int 16:1713–1720 de Liefde II, van der KM, de Laet CE et al (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporosis Int 16:1713–1720
30.
go back to reference Schwartz AV, Sellmeyer DE, Strotmeyer ES et al (2005) Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596–603PubMed Schwartz AV, Sellmeyer DE, Strotmeyer ES et al (2005) Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596–603PubMed
31.
go back to reference Strotmeyer ES, Cauley JA, Schwartz AV et al (2004) 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 19:1084–1091PubMed Strotmeyer ES, Cauley JA, Schwartz AV et al (2004) 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 19:1084–1091PubMed
32.
go back to reference Blake GM, Wahner HW, Fogelman I (1999) The evaluation of osteoporosis: dual energy X-ray absorptiometry and ultrasound in clinical practice. Martin Dunitz, London Blake GM, Wahner HW, Fogelman I (1999) The evaluation of osteoporosis: dual energy X-ray absorptiometry and ultrasound in clinical practice. Martin Dunitz, London
33.
go back to reference Jadad AR, Moore RA, Carroll D et al (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12PubMed Jadad AR, Moore RA, Carroll D et al (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12PubMed
34.
go back to reference Böhning D (2000) Computer-assisted analysis of mixtures and applications: Meta-analysis, disease mapping and others. Chapman&Hall/CRC, Boca Raton Böhning D (2000) Computer-assisted analysis of mixtures and applications: Meta-analysis, disease mapping and others. Chapman&Hall/CRC, Boca Raton
35.
go back to reference Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259PubMed Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259PubMed
36.
go back to reference Stata Statistical Software: Release 8.0 (2003). STATACorp., College Station, TX Stata Statistical Software: Release 8.0 (2003). STATACorp., College Station, TX
37.
go back to reference Miao J, Brismar K, Nyren O et al (2005) Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in sweden. Diabetes Care 28:2850–2855PubMed Miao J, Brismar K, Nyren O et al (2005) Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in sweden. Diabetes Care 28:2850–2855PubMed
38.
go back to reference Vestergaard P, Rejnmark L, Mosekilde L (2005) Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48:1292–1299PubMed Vestergaard P, Rejnmark L, Mosekilde L (2005) Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48:1292–1299PubMed
39.
go back to reference Gerdhem P, Isaksson A, Åkesson K et al (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporosis Int 16:1506–1512 Gerdhem P, Isaksson A, Åkesson K et al (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporosis Int 16:1506–1512
40.
go back to reference Clausen P, Feldt-Rasmussen B, Jacobsen P et al (1997) Microalbuminuria as an early indicator of osteopenia in male insulin-dependent diabetic patients. Diabet Med 14:1038–1043PubMed Clausen P, Feldt-Rasmussen B, Jacobsen P et al (1997) Microalbuminuria as an early indicator of osteopenia in male insulin-dependent diabetic patients. Diabet Med 14:1038–1043PubMed
41.
go back to reference Goliat E, Marusza W, Ostrowski K et al (1998) [Microalbuminuria as a risk factor for diabetic osteopathy in patients with IDDM and renal sufficiency]. Pol Arch Med Wewn 100:111–118PubMed Goliat E, Marusza W, Ostrowski K et al (1998) [Microalbuminuria as a risk factor for diabetic osteopathy in patients with IDDM and renal sufficiency]. Pol Arch Med Wewn 100:111–118PubMed
42.
go back to reference Ivers RQ, Mitchell P, Cumming RG et al (2001) Diabetes and risk of fractures-the blue mountains eye study. Diabetes Care 24:1198–1203PubMed Ivers RQ, Mitchell P, Cumming RG et al (2001) Diabetes and risk of fractures-the blue mountains eye study. Diabetes Care 24:1198–1203PubMed
43.
go back to reference Strotmeyer ES, Cauley JA, Schwartz AV et al (2005) 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 165:1612–1617PubMed Strotmeyer ES, Cauley JA, Schwartz AV et al (2005) 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 165:1612–1617PubMed
44.
go back to reference De Laet C, Kanis JA, Oden A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporosis Int 16:1330–1338 De Laet C, Kanis JA, Oden A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporosis Int 16:1330–1338
45.
go back to reference Vestergaard P (2005) Anti-resorptive therapy for the prevention of postmenopausal osteoporosis : when should treatment begin? Treat Endocrinol 4:263–277PubMed Vestergaard P (2005) Anti-resorptive therapy for the prevention of postmenopausal osteoporosis : when should treatment begin? Treat Endocrinol 4:263–277PubMed
46.
go back to reference Ahmed LA, Joakimsen RM, Berntsen GK et al (2005) Diabetes mellitus and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int1-6 Ahmed LA, Joakimsen RM, Berntsen GK et al (2005) Diabetes mellitus and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int1-6
47.
go back to reference van Beresteijn ECH, van Laarhoven JPRM, Smals AGH (1992) Body weight and/or endogenous estradiol as determinants of cortical bone mass and bone loss in healthy early postmenopausal women. Acta Endocrinol 127:226–230PubMed van Beresteijn ECH, van Laarhoven JPRM, Smals AGH (1992) Body weight and/or endogenous estradiol as determinants of cortical bone mass and bone loss in healthy early postmenopausal women. Acta Endocrinol 127:226–230PubMed
48.
go back to reference Cortes-Sancho R, Perez-Castrillon JL, Martin-Escudero JC et al (2004) Type 2 diabetes mellitus as a risk factor for hip fracture. J Am Geriatr Soc 52:1778–1779PubMed Cortes-Sancho R, Perez-Castrillon JL, Martin-Escudero JC et al (2004) Type 2 diabetes mellitus as a risk factor for hip fracture. J Am Geriatr Soc 52:1778–1779PubMed
49.
go back to reference Hanley DA, Brown JP, Tenenhouse A et al (2003) 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 18:784–790PubMed Hanley DA, Brown JP, Tenenhouse A et al (2003) 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 18:784–790PubMed
50.
go back to reference Michaelsson K, Holmberg L, Mallmin H et al (1995) Diet and hip fracture risk: a case-control study. Study Group of the Multiple Risk Survey on Swedish Women for Eating Assessment. Int J Epidemiol 24:771–782PubMed Michaelsson K, Holmberg L, Mallmin H et al (1995) Diet and hip fracture risk: a case-control study. Study Group of the Multiple Risk Survey on Swedish Women for Eating Assessment. Int J Epidemiol 24:771–782PubMed
51.
go back to reference Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMed Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMed
52.
go back to reference Poor G, Atkinson EJ, O’Fallon WM et al (1995) Predictors of hip-fractures in elderly men. J Bone Miner Res 10:1900–1907PubMed Poor G, Atkinson EJ, O’Fallon WM et al (1995) Predictors of hip-fractures in elderly men. J Bone Miner Res 10:1900–1907PubMed
53.
go back to reference Seeley DG, Kelsey J, Jergas M et al (1996) Predictors of ankle and foot fractures in older women. The Study of Osteoporotic Fractures Research Group. J Bone Miner Res 11:1347–1355PubMed Seeley DG, Kelsey J, Jergas M et al (1996) Predictors of ankle and foot fractures in older women. The Study of Osteoporotic Fractures Research Group. J Bone Miner Res 11:1347–1355PubMed
54.
go back to reference Taylor BC, Schreiner PJ, Stone KL et al (2004) Long-term prediction of incident hip fracture risk in elderly white women: study of osteoporotic fractures. J Am Geriatr Soc 52:1479–1486PubMed Taylor BC, Schreiner PJ, Stone KL et al (2004) Long-term prediction of incident hip fracture risk in elderly white women: study of osteoporotic fractures. J Am Geriatr Soc 52:1479–1486PubMed
55.
go back to reference van Daele PL, Stolk RP, Burger H et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study [see comments]. Ann Intern Med 122:409–414PubMed van Daele PL, Stolk RP, Burger H et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study [see comments]. Ann Intern Med 122:409–414PubMed
56.
go back to reference Akin O, Gol K, Akturk M et al (2003) Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol 17:19–29PubMed Akin O, Gol K, Akturk M et al (2003) Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol 17:19–29PubMed
57.
go back to reference Al Maatouq MA, El Desouki MI, Othman SA et al (2004) Prevalence of osteoporosis among postmenopausal females with diabetes mellitus. Saudi Med J 25:1423–1427 Al Maatouq MA, El Desouki MI, Othman SA et al (2004) Prevalence of osteoporosis among postmenopausal females with diabetes mellitus. Saudi Med J 25:1423–1427
58.
go back to reference Altamirano E, Nelly A, delaLuz PM et al (1997) Bone mineral content and bone mineral density in children with insulin-dependent diabetes mellitus. J Bone Miner Res 12:S653 Altamirano E, Nelly A, delaLuz PM et al (1997) Bone mineral content and bone mineral density in children with insulin-dependent diabetes mellitus. J Bone Miner Res 12:S653
59.
go back to reference Aoki TT, Grecu EO, Arcangeli MA (1996) Lumbar spine bone mineral density in diabetes mellitus. J Invest Med 44:A127 Aoki TT, Grecu EO, Arcangeli MA (1996) Lumbar spine bone mineral density in diabetes mellitus. J Invest Med 44:A127
60.
go back to reference Barret-Connor E, Holbrook TL (1992) Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337 Barret-Connor E, Holbrook TL (1992) Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337
61.
go back to reference Barros H, Pereira S, Marantes I et al (2003) Bone mineral density and diabetes mellitus type 2 in post-menopausal women. Ann Rheum Dis 62:317–318 Barros H, Pereira S, Marantes I et al (2003) Bone mineral density and diabetes mellitus type 2 in post-menopausal women. Ann Rheum Dis 62:317–318
62.
go back to reference Buysschaert M, Cauwe F, Jamart J et al (1992) Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab 18:32–37PubMed Buysschaert M, Cauwe F, Jamart J et al (1992) Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab 18:32–37PubMed
63.
go back to reference Campos Pastor MM, Lopez-Ibarra PJ, Escobar-Jimenez F et al (2000) Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int 11:455–459PubMed Campos Pastor MM, Lopez-Ibarra PJ, Escobar-Jimenez F et al (2000) Intensive insulin therapy and bone mineral density in type 1 diabetes mellitus: a prospective study. Osteoporos Int 11:455–459PubMed
64.
go back to reference Chen Y, Kang H, Mao S et al (2003) Measurement of bone mineral density in patients with type 2 diabetes mellitus. Chinese Journal of Clinical Rehabilitation 7:514–515 Chen Y, Kang H, Mao S et al (2003) Measurement of bone mineral density in patients with type 2 diabetes mellitus. Chinese Journal of Clinical Rehabilitation 7:514–515
65.
go back to reference Chung YS, Lee MD, Lee SK et al (2000) HMG-CoA reductase inhibitors increase BMD in type 2 diabetes mellitus patients. J Clin Endocrinol Metab 85:1137–1142PubMed Chung YS, Lee MD, Lee SK et al (2000) HMG-CoA reductase inhibitors increase BMD in type 2 diabetes mellitus patients. J Clin Endocrinol Metab 85:1137–1142PubMed
66.
go back to reference Compston JE, Smith EM, Matthews C et al (1994) Whole body composition and regional bone mass in women with insulin-dependent diabetes mellitus. Clin Endocrinol (Oxf) 41:289–293 Compston JE, Smith EM, Matthews C et al (1994) Whole body composition and regional bone mass in women with insulin-dependent diabetes mellitus. Clin Endocrinol (Oxf) 41:289–293
67.
go back to reference De Schepper J, Smitz J, Rosseneu S et al (1998) Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 50:193–196PubMed De Schepper J, Smitz J, Rosseneu S et al (1998) Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 50:193–196PubMed
68.
go back to reference Dennison EM, Syddall HE, Aihie SA et al (2004) 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 47:1963–1968PubMed Dennison EM, Syddall HE, Aihie SA et al (2004) 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 47:1963–1968PubMed
69.
go back to reference Ersoy B, Goksen D, Darcan S et al (1999) Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66:375–379PubMed Ersoy B, Goksen D, Darcan S et al (1999) Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66:375–379PubMed
70.
go back to reference Fei ZX, Zhang ZS (2004) Correlation analysis of bone mineral density with serum insulin, HbA1C and body mass index in patients with diabetes mellitus. Chinese Journal of Clinical Rehabilitation 8:2898–2899 Fei ZX, Zhang ZS (2004) Correlation analysis of bone mineral density with serum insulin, HbA1C and body mass index in patients with diabetes mellitus. Chinese Journal of Clinical Rehabilitation 8:2898–2899
71.
go back to reference Forst T, Pfutzner A, Kann P et al (1995) Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 12:874–879PubMedCrossRef Forst T, Pfutzner A, Kann P et al (1995) Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 12:874–879PubMedCrossRef
72.
go back to reference Gunczler P, Lanes R, Paoli M et al (2001) Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14:525–528PubMed Gunczler P, Lanes R, Paoli M et al (2001) Decreased bone mineral density and bone formation markers shortly after diagnosis of clinical type 1 diabetes mellitus. J Pediatr Endocrinol Metab 14:525–528PubMed
73.
go back to reference Hadjidakis D, Kokkinakis E, Giannopoulos G et al (1994) Bone mineral density in type II diabetes. Diabetologia 37:A149 Hadjidakis D, Kokkinakis E, Giannopoulos G et al (1994) Bone mineral density in type II diabetes. Diabetologia 37:A149
74.
go back to reference Hadjidakis D, Mylonakis A, Raptis A et al (2004) Does Type 2 diabetes influence the bone mineral density of women after surgically induced menopause? Diabetologia 47:A330 Hadjidakis D, Mylonakis A, Raptis A et al (2004) Does Type 2 diabetes influence the bone mineral density of women after surgically induced menopause? Diabetologia 47:A330
75.
go back to reference Hadjidakis DJ, Katsavochristos P, Mylonakis A et al (2003) The influence of diabetes mellitus Type 2 on bone mineral density of premenopausal women. Diabetologia 46:A233 Hadjidakis DJ, Katsavochristos P, Mylonakis A et al (2003) The influence of diabetes mellitus Type 2 on bone mineral density of premenopausal women. Diabetologia 46:A233
76.
go back to reference Hadjidakis DJ, Mylonakis AM, Sfakianakis ME et al (2005) Diabetes and premature menopause: is their co-existence detrimental to the skeleton? Eur J Endocrinol 152:437–442PubMed Hadjidakis DJ, Mylonakis AM, Sfakianakis ME et al (2005) Diabetes and premature menopause: is their co-existence detrimental to the skeleton? Eur J Endocrinol 152:437–442PubMed
77.
go back to reference Hauache OM, Lazaretti-Castro M, Andreoni S et al (1998) Vitamin D receptor gene polymorphism: correlation with bone mineral density in a Brazilian population with insulin-dependent diabetes mellitus. Osteoporos Int 8:204–210PubMed Hauache OM, Lazaretti-Castro M, Andreoni S et al (1998) Vitamin D receptor gene polymorphism: correlation with bone mineral density in a Brazilian population with insulin-dependent diabetes mellitus. Osteoporos Int 8:204–210PubMed
78.
go back to reference Heap J, Murray MA, Miller SC et al (2004) Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr 144:56–62PubMed Heap J, Murray MA, Miller SC et al (2004) Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr 144:56–62PubMed
79.
go back to reference Hong SK, Lee MK, Lee MS et al (1990) Bone mineral density in diabetic patients. Recent advances in insulin therapy: proceedings of the 5th Korea-Japan Symposium on Diabetes Mellitus. ICS867, The 5th Korea-Japan Symposium on Diabetes Mellitus, Chejodo, JAPAN, 27 APR to 28 APR 89, ISBN 0444811311, Editors Lee T.H., Huh K.B., Baba S.295–298 Hong SK, Lee MK, Lee MS et al (1990) Bone mineral density in diabetic patients. Recent advances in insulin therapy: proceedings of the 5th Korea-Japan Symposium on Diabetes Mellitus. ICS867, The 5th Korea-Japan Symposium on Diabetes Mellitus, Chejodo, JAPAN, 27 APR to 28 APR 89, ISBN 0444811311, Editors Lee T.H., Huh K.B., Baba S.295–298
80.
go back to reference Horiuchi T, Nakamura T, Miyao M et al (1995) [Bone mineral density in postmenopausal elderly women with type 2 diabetes]. Nippon Ronen Igakkai Zasshi 32:756–760PubMed Horiuchi T, Nakamura T, Miyao M et al (1995) [Bone mineral density in postmenopausal elderly women with type 2 diabetes]. Nippon Ronen Igakkai Zasshi 32:756–760PubMed
81.
go back to reference Ingberg CM, Palmer M, Aman J et al (2004) Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255:392–398PubMed Ingberg CM, Palmer M, Aman J et al (2004) Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255:392–398PubMed
82.
go back to reference Isaia GC, Ardissone P, di Stefano M et al (1999) Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 36:35–38PubMed Isaia GC, Ardissone P, di Stefano M et al (1999) Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 36:35–38PubMed
83.
go back to reference Kao WH, Kammerer CM, Schneider JL et al (2003) Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res 34:399–406PubMed Kao WH, Kammerer CM, Schneider JL et al (2003) Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res 34:399–406PubMed
84.
go back to reference Kayath MJ, Dib SA, Vieiaa JG (1994) Prevalence and magnitude of osteopenia associated with insulin-dependent diabetes mellitus. J Diabetes Complications 8:97–104PubMed Kayath MJ, Dib SA, Vieiaa JG (1994) Prevalence and magnitude of osteopenia associated with insulin-dependent diabetes mellitus. J Diabetes Complications 8:97–104PubMed
85.
go back to reference Kemink SA, Hermus AR, Swinkels LM et al (2000) Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23:295–303PubMed Kemink SA, Hermus AR, Swinkels LM et al (2000) Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23:295–303PubMed
86.
go back to reference Kuo SW, Huang WS, Jeng CY et al (1998) Bone mineral density in patients with insulin-dependent diabetes mellitus. J Nuclear Med 39:194P Kuo SW, Huang WS, Jeng CY et al (1998) Bone mineral density in patients with insulin-dependent diabetes mellitus. J Nuclear Med 39:194P
87.
go back to reference Liu EY, Wactawski-Wende J, Donahue RP et al (2003) Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care 26:2365–2369PubMed Liu EY, Wactawski-Wende J, Donahue RP et al (2003) Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care 26:2365–2369PubMed
88.
go back to reference Lopez-Ibarra PJ, Pastor MM, Escobar-Jimenez F et al (2001) Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract 7:346–351PubMed Lopez-Ibarra PJ, Pastor MM, Escobar-Jimenez F et al (2001) Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract 7:346–351PubMed
89.
go back to reference Lunt M, Masaryk P, Scheidt-Nave C et al (2001) The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS study. Osteoporos Int 12:688–698PubMed Lunt M, Masaryk P, Scheidt-Nave C et al (2001) The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS study. Osteoporos Int 12:688–698PubMed
90.
go back to reference Lunt H, Florkowski CM, Cook HB et al (2001) Bone mineral density, type 1 diabetes, and celiac disease. Diabetes Care 24:791–792PubMed Lunt H, Florkowski CM, Cook HB et al (2001) Bone mineral density, type 1 diabetes, and celiac disease. Diabetes Care 24:791–792PubMed
91.
go back to reference Majima T, Komatsu Y, Yamada T et al (2005) Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporosis Int 16:907–913 Majima T, Komatsu Y, Yamada T et al (2005) Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporosis Int 16:907–913
92.
go back to reference Maugeri D, Panebianco P, Rosso D et al (2002) Alendronate reduces the daily consumption of insulin (DCI) in patients with senile type I diabetes and osteoporosis. Arch Gerontol Geriatr 34:117–122PubMed Maugeri D, Panebianco P, Rosso D et al (2002) Alendronate reduces the daily consumption of insulin (DCI) in patients with senile type I diabetes and osteoporosis. Arch Gerontol Geriatr 34:117–122PubMed
93.
go back to reference Miazgowski T, Andrysiak-Mamos E, Pynka S et al (1997) [The evaluation of bone mineral density and selected markers of bone turnover in patients with insulin dependent diabetes mellitus]. Przegl Lek 54:533–539PubMed Miazgowski T, Andrysiak-Mamos E, Pynka S et al (1997) [The evaluation of bone mineral density and selected markers of bone turnover in patients with insulin dependent diabetes mellitus]. Przegl Lek 54:533–539PubMed
94.
go back to reference Moyer-Mileur LJ, Dixon SB, Quick JL et al (2004) Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr 145:662–669PubMed Moyer-Mileur LJ, Dixon SB, Quick JL et al (2004) Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr 145:662–669PubMed
95.
go back to reference Munoz-Torres M, Jodar E, Escobar-Jimenez F et al (1996) Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int 58:316–319PubMedCrossRef Munoz-Torres M, Jodar E, Escobar-Jimenez F et al (1996) Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int 58:316–319PubMedCrossRef
96.
go back to reference Olmos JM, Perez-Castrillon JL, Garcia MT et al (1994) Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner 26:1–8PubMedCrossRef Olmos JM, Perez-Castrillon JL, Garcia MT et al (1994) Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner 26:1–8PubMedCrossRef
97.
go back to reference Pascual J, Argente J, Lopez MB et al (1998) Bone mineral density in children and adolescents with diabetes mellitus type 1 of recent onset. Calcif Tissue Int 62:31–35PubMed Pascual J, Argente J, Lopez MB et al (1998) Bone mineral density in children and adolescents with diabetes mellitus type 1 of recent onset. Calcif Tissue Int 62:31–35PubMed
98.
go back to reference Rachon D, Mysliwska J, Suchecka-Rachon K et al (2003) Serum interleukin-6 levels and bone mineral density at the femoral neck in post-menopausal women with Type 1 diabetes. Diabet Med 20:475–480PubMed Rachon D, Mysliwska J, Suchecka-Rachon K et al (2003) Serum interleukin-6 levels and bone mineral density at the femoral neck in post-menopausal women with Type 1 diabetes. Diabet Med 20:475–480PubMed
99.
go back to reference Rishaug U, Birkeland KI, Falch JA et al (1995) Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest 55:257–262PubMed Rishaug U, Birkeland KI, Falch JA et al (1995) Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest 55:257–262PubMed
100.
go back to reference Rozadilla A, Nolla JM, Montana E et al (2000) Bone mineral density in patients with type 1 diabetes mellitus. Joint Bone Spine 67:215–218PubMed Rozadilla A, Nolla JM, Montana E et al (2000) Bone mineral density in patients with type 1 diabetes mellitus. Joint Bone Spine 67:215–218PubMed
101.
go back to reference Sahin G, Bagis S, Cimen OB et al (2001) Lumbar and femoral bone mineral density in type 2 Turkish diabetic patients. Acta Medica (Hradec.Kralove) 44:141–143 Sahin G, Bagis S, Cimen OB et al (2001) Lumbar and femoral bone mineral density in type 2 Turkish diabetic patients. Acta Medica (Hradec.Kralove) 44:141–143
102.
go back to reference Sahin G, Polat G, Bagis S et al (2002) Study of axial bone mineral density in postmenopausal women with diffuse idiopathic skeletal hyperostosis related to type 2 diabetes mellitus. J Womens Health (Larchmt) 11:801–804CrossRef Sahin G, Polat G, Bagis S et al (2002) Study of axial bone mineral density in postmenopausal women with diffuse idiopathic skeletal hyperostosis related to type 2 diabetes mellitus. J Womens Health (Larchmt) 11:801–804CrossRef
103.
go back to reference Schwartz AV, Sellmeyer DE, Ensrud KE et al (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38PubMed Schwartz AV, Sellmeyer DE, Ensrud KE et al (2001) Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32–38PubMed
104.
go back to reference Sert M, Tetiker T, Kirim S et al (2003) Type 2 diabetes mellitus and osteopenia: is there an association? Acta Diabetol 40:105–108PubMed Sert M, Tetiker T, Kirim S et al (2003) Type 2 diabetes mellitus and osteopenia: is there an association? Acta Diabetol 40:105–108PubMed
105.
go back to reference Sosa M, Dominguez M, Navarro MC et al (1996) Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10:201–205PubMed Sosa M, Dominguez M, Navarro MC et al (1996) Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10:201–205PubMed
106.
go back to reference Strotmeyer E, Cauley J, Dorman J (2003) Women with type 1 diabetes have lower bone mineral density (BMD) than women without diabetes. Diabetes 52:A41 Strotmeyer E, Cauley J, Dorman J (2003) Women with type 1 diabetes have lower bone mineral density (BMD) than women without diabetes. Diabetes 52:A41
107.
go back to reference Valerio G, del Puente A, Esposito-del Puente A et al (2002) The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 58:266–272PubMed Valerio G, del Puente A, Esposito-del Puente A et al (2002) The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 58:266–272PubMed
108.
go back to reference Vargas DM, Rigotti T, Gutz CN et al (2003) [Bone mineralization in children and adolescents with type 1 diabetes]. J Pediatr (Rio J) 79:253–258 Vargas DM, Rigotti T, Gutz CN et al (2003) [Bone mineralization in children and adolescents with type 1 diabetes]. J Pediatr (Rio J) 79:253–258
109.
go back to reference Vina SE, Bueno LG, Armada Maresca MI et al (2000) [Bone mineral density in juvenile-onset diabetes mellitus]. An Esp Pediatr 52:507–515 Vina SE, Bueno LG, Armada Maresca MI et al (2000) [Bone mineral density in juvenile-onset diabetes mellitus]. An Esp Pediatr 52:507–515
110.
go back to reference Weinstock RS, Goland RS, Shane E et al (1989) Bone mineral density in women with type II diabetes mellitus. J Bone Mineral Res 4:97–101CrossRef Weinstock RS, Goland RS, Shane E et al (1989) Bone mineral density in women with type II diabetes mellitus. J Bone Mineral Res 4:97–101CrossRef
111.
go back to reference Yang S, Xu XG, Yue GY (2004) Characteristics of bone mineral density loss in type 2 diabetic patients. Chinese Journal of Clinical Rehabilitation 8:1010–1011 Yang S, Xu XG, Yue GY (2004) Characteristics of bone mineral density loss in type 2 diabetic patients. Chinese Journal of Clinical Rehabilitation 8:1010–1011
Metadata
Title
Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis
Author
P. Vestergaard
Publication date
01-04-2007
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 4/2007
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-006-0253-4

Other articles of this Issue 4/2007

Osteoporosis International 4/2007 Go to the issue