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

McNair P, Madsbad S, Christensen MS et al (1979) Bone mineral loss in insulin-treated diabetes mellitus: studies on pathogenesis. Acta Endocrinol 90:463–472

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 11:55–59

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 42:920–925

Raskin P, Stevenson MRM, Barilla DE et al (1978) The hypercalciuria of diabetes mellitus: its amelioration with insulin. Clin Endocrinol 9:329–335

McNair P, Christensen MS, Madsbad S et al (1981) Hypoparathyroidism in diabetes mellitus. Acta Endocrinol (Copenh) 96:81–86

Bouillon R (1991) Diabetic bone disease [editorial]. Calcif Tissue Int 49:155–160

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 159:297–306

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, 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 65:101–104

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 8:260–270

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):54–57

Odetti P, Rossi S, Monacelli F et al (2005) Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci 1043:710–717

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

Yamagishi S, Nakamura K, Inoue H (2005) Possible participation of advanced glycation end products in the pathogenesis of osteoporosis in diabetic patients. Medical Hypotheses 65:1013–1015

Cozen L (1972) Does diabetes delay fracture healing? Clin Orthop 82:134–140

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 76:256–260

Nisbeth U, Lindh E, Ljunghall S et al (1999) Increased fracture rate in diabetes mellitus and females after renal transplantation. Transplantation 67:1218–1222

Rix M, Andreassen H, Eskildsen P (1999) Impact of peripheral neuropathy on bone density in patients with type 1 diabetes. Diabetes Care 22:827–831

McNair P, Christensen MS, Christiansen C et al (1981) Is diabetic osteoporosis due to microangiopathy? Lancet 1:1271

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 12:283–289

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

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 60:1157–1162

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 52:660–666

Nabarro JD (1985) Compression fractures of the dorsal spine in hypoglycaemic fits in diabetes. Br Med J (Clin Res Ed) 291:1320

Pal B (1985) Compression fractures of the dorsal spine in hypoglycemic fits in diabetes. Br Med J (Clin Res Ed) 291:1646

Tuominen JT, Impivaara O, Puukka P et al (1999) Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200

van Daele PL, Stolk RP, Burger H et al (1995) Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med 122:409–414

Heath III H, Melton III LJ, Chu CP (1980) Diabetes mellitus and risk of skeletal fracture. N Engl J Med 303:567–570

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

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 20:596–603

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 19:1084–1091

Blake GM, Wahner HW, Fogelman I (1999) The evaluation of osteoporosis: dual energy X-ray absorptiometry and ultrasound in clinical practice. Martin Dunitz, London

Jadad AR, Moore RA, Carroll D et al (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12

Böhning D (2000) Computer-assisted analysis of mixtures and applications: Meta-analysis, disease mapping and others. Chapman&Hall/CRC, Boca Raton

Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259

Stata Statistical Software: Release 8.0 (2003). STATACorp., College Station, TX

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 28:2850–2855

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 48:1292–1299

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

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 14:1038–1043

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 100:111–118

Ivers RQ, Mitchell P, Cumming RG et al (2001) Diabetes and risk of fractures-the blue mountains eye study. Diabetes Care 24:1198–1203

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 165:1612–1617

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

Vestergaard P (2005) Anti-resorptive therapy for the prevention of postmenopausal osteoporosis : when should treatment begin? Treat Endocrinol 4:263–277

Ahmed LA, Joakimsen RM, Berntsen GK et al (2005) Diabetes mellitus and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int1-6

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 127:226–230

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 52:1778–1779

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 18:784–790

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 24:771–782

Nicodemus KK, Folsom AR (2001) Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197

Poor G, Atkinson EJ, O’Fallon WM et al (1995) Predictors of hip-fractures in elderly men. J Bone Miner Res 10:1900–1907

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 11:1347–1355

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 52:1479–1486

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 122:409–414

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 17:19–29

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

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

Aoki TT, Grecu EO, Arcangeli MA (1996) Lumbar spine bone mineral density in diabetes mellitus. J Invest Med 44:A127

Barret-Connor E, Holbrook TL (1992) Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA 268:3333–3337

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

Buysschaert M, Cauwe F, Jamart J et al (1992) Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab 18:32–37

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 11:455–459

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

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 85:1137–1142

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

De Schepper J, Smitz J, Rosseneu S et al (1998) Lumbar spine bone mineral density in diabetic children with recent onset. Horm Res 50:193–196

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 47:1963–1968

Ersoy B, Goksen D, Darcan S et al (1999) Evaluation of bone mineral density in children with diabetes mellitus. Indian J Pediatr 66:375–379

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

Forst T, Pfutzner A, Kann P et al (1995) Peripheral osteopenia in adult patients with insulin-dependent diabetes mellitus. Diabet Med 12:874–879

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 14:525–528

Hadjidakis D, Kokkinakis E, Giannopoulos G et al (1994) Bone mineral density in type II diabetes. Diabetologia 37:A149

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 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, Mylonakis AM, Sfakianakis ME et al (2005) Diabetes and premature menopause: is their co-existence detrimental to the skeleton? Eur J Endocrinol 152:437–442

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 8:204–210

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 144:56–62

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

Horiuchi T, Nakamura T, Miyao M et al (1995) [Bone mineral density in postmenopausal elderly women with type 2 diabetes]. Nippon Ronen Igakkai Zasshi 32:756–760

Ingberg CM, Palmer M, Aman J et al (2004) Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255:392–398

Isaia GC, Ardissone P, di Stefano M et al (1999) Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 36:35–38

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 34:399–406

Kayath MJ, Dib SA, Vieiaa JG (1994) Prevalence and magnitude of osteopenia associated with insulin-dependent diabetes mellitus. J Diabetes Complications 8:97–104

Kemink SA, Hermus AR, Swinkels LM et al (2000) Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23:295–303

Kuo SW, Huang WS, Jeng CY et al (1998) Bone mineral density in patients with insulin-dependent diabetes mellitus. J Nuclear Med 39:194P

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 26:2365–2369

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 7:346–351

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 12:688–698

Lunt H, Florkowski CM, Cook HB et al (2001) Bone mineral density, type 1 diabetes, and celiac disease. Diabetes Care 24:791–792

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

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 34:117–122

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 54:533–539

Moyer-Mileur LJ, Dixon SB, Quick JL et al (2004) Bone mineral acquisition in adolescents with type 1 diabetes. J Pediatr 145:662–669

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 58:316–319

Olmos JM, Perez-Castrillon JL, Garcia MT et al (1994) Bone densitometry and biochemical bone remodeling markers in type 1 diabetes mellitus. Bone Miner 26:1–8

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 62:31–35

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 20:475–480

Rishaug U, Birkeland KI, Falch JA et al (1995) Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest 55:257–262

Rozadilla A, Nolla JM, Montana E et al (2000) Bone mineral density in patients with type 1 diabetes mellitus. Joint Bone Spine 67:215–218

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, 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) 11:801–804

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 86:32–38

Sert M, Tetiker T, Kirim S et al (2003) Type 2 diabetes mellitus and osteopenia: is there an association? Acta Diabetol 40:105–108

Sosa M, Dominguez M, Navarro MC et al (1996) Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications 10:201–205

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

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 58:266–272

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

Vina SE, Bueno LG, Armada Maresca MI et al (2000) [Bone mineral density in juvenile-onset diabetes mellitus]. An Esp Pediatr 52:507–515

Weinstock RS, Goland RS, Shane E et al (1989) Bone mineral density in women with type II diabetes mellitus. J Bone Mineral Res 4:97–101

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