Skip to main content
Top
Published in: European Journal of Epidemiology 5/2012

Open Access 01-05-2012 | REVIEW

Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies

Authors: Lili Ma, Ling Oei, Lindi Jiang, Karol Estrada, Huiyong Chen, Zhen Wang, Qiang Yu, Maria Carola Zillikens, Xin Gao, Fernando Rivadeneira

Published in: European Journal of Epidemiology | Issue 5/2012

Login to get access

Abstract

Type 2 diabetes mellitus (T2DM) influences bone metabolism, but the relation of T2DM with bone mineral density (BMD) remains inconsistent across studies. The objective of this study was to perform a meta-analysis and meta-regression of the literature to estimate the difference in BMD (g/cm2) between diabetic and non-diabetic populations, and to investigate potential underlying mechanisms. A literature search was performed in PubMed and Ovid extracting data from articles prior to May 2010. Eligible studies were those where the association between T2DM and BMD measured by dual energy X-ray absorptiometry was evaluated using a cross-sectional, cohort or case–control design, including both healthy controls and subjects with T2DM. The analysis was done on 15 observational studies (3,437 diabetics and 19,139 controls). Meta-analysis showed that BMD in diabetics was significantly higher, with pooled mean differences of 0.04 (95% CI: 0.02, 0.05) at the femoral neck, 0.06 (95% CI: 0.04, 0.08) at the hip and 0.06 (95% CI: 0.04, 0.07) at the spine. The differences for forearm BMD were not significantly different between diabetics and non-diabetics. Sex-stratified analyses showed similar results in both genders. Substantial heterogeneity was found to originate from differences in study design and possibly diabetes definition. Also, by applying meta-regression we could establish that younger age, male gender, higher body mass index and higher HbA1C were positively associated with higher BMD levels in diabetic individuals. We conclude that individuals with T2DM from both genders have higher BMD levels, but that multiple factors influence BMD in individuals with T2DM.
Literature
1.
go back to reference Albright F, Reifenstein EC. The parathyroid glands and metabolic bone disease: selected studies. Baltimore: Williams and Wilkins; 1948. Albright F, Reifenstein EC. The parathyroid glands and metabolic bone disease: selected studies. Baltimore: Williams and Wilkins; 1948.
3.
go back to reference Saller A, Maggi S, Romanato G, Tonin P, Crepaldi G. Diabetes and osteoporosis. Aging Clin Exp Res. 2008;20(18852539):280–9.PubMed Saller A, Maggi S, Romanato G, Tonin P, Crepaldi G. Diabetes and osteoporosis. Aging Clin Exp Res. 2008;20(18852539):280–9.PubMed
4.
go back to reference van Daele PL, Stolk RP, Burger H, et al. Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med. 1995;122(7856988):409–14.PubMed van Daele PL, Stolk RP, Burger H, et al. Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann Intern Med. 1995;122(7856988):409–14.PubMed
5.
go back to reference Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2009;15(19114969):5–9. Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2009;15(19114969):5–9.
6.
go back to reference Kao WHL, Kammerer CM, Schneider JL, Bauer RL, Mitchell BD. Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res. 2003;34(14602507):399–406.PubMed Kao WHL, Kammerer CM, Schneider JL, Bauer RL, Mitchell BD. Type 2 diabetes is associated with increased bone mineral density in Mexican-American women. Arch Med Res. 2003;34(14602507):399–406.PubMed
7.
go back to reference Majima T, Komatsu Y, Yamada T, et al. Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int. 2005;16(15558237):907–13.PubMedCrossRef Majima T, Komatsu Y, Yamada T, et al. Decreased bone mineral density at the distal radius, but not at the lumbar spine or the femoral neck, in Japanese type 2 diabetic patients. Osteoporos Int. 2005;16(15558237):907–13.PubMedCrossRef
8.
go back to reference Kahn A, Gibbons R, Perkins S, Gazit D. Age-related bone loss. A hypothesis and initial assessment in mice. Clin Orthop Relat Res. 1995;7641500:69–75. Kahn A, Gibbons R, Perkins S, Gazit D. Age-related bone loss. A hypothesis and initial assessment in mice. Clin Orthop Relat Res. 1995;7641500:69–75.
9.
go back to reference Min J-Y, Min K-B, Paek D, Kang D, Cho S-I. Age curves of bone mineral density at the distal radius and calcaneus in Koreans. J Bone Miner Metab. 2010;28(19634016):94–9100.PubMedCrossRef Min J-Y, Min K-B, Paek D, Kang D, Cho S-I. Age curves of bone mineral density at the distal radius and calcaneus in Koreans. J Bone Miner Metab. 2010;28(19634016):94–9100.PubMedCrossRef
10.
go back to reference Tung S, Iqbal J. Evolution, aging, and osteoporosis. Ann N Y Acad Sci. 2007;1116(18083942):499–506.PubMedCrossRef Tung S, Iqbal J. Evolution, aging, and osteoporosis. Ann N Y Acad Sci. 2007;1116(18083942):499–506.PubMedCrossRef
11.
go back to reference Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA. 1992;268(1453525):3333–7.PubMedCrossRef Barrett-Connor E, Holbrook TL. Sex differences in osteoporosis in older adults with non-insulin-dependent diabetes mellitus. JAMA. 1992;268(1453525):3333–7.PubMedCrossRef
12.
go back to reference Gerdhem P, Isaksson A, Akesson K, Obrant KJ. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int. 2005;16(12):1506–12. doi:10.1007/s00198-005-1877-5.PubMedCrossRef Gerdhem P, Isaksson A, Akesson K, Obrant KJ. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int. 2005;16(12):1506–12. doi:10.​1007/​s00198-005-1877-5.PubMedCrossRef
13.
go back to reference Schwartz AV, Sellmeyer DE, Ensrud KE, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(11231974):32–8.PubMedCrossRef Schwartz AV, Sellmeyer DE, Ensrud KE, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(11231974):32–8.PubMedCrossRef
14.
go back to reference de Liefde II, van der Klift M, de Laet CEDH, van Daele PLA, Hofman A, Pols HAP. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int. 2005;16(15940395):1713–20.PubMedCrossRef de Liefde II, van der Klift M, de Laet CEDH, van Daele PLA, Hofman A, Pols HAP. Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int. 2005;16(15940395):1713–20.PubMedCrossRef
15.
go back to reference Strotmeyer ES, Cauley JA, Schwartz AV, et al. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165(16043679):1612–7.PubMedCrossRef Strotmeyer ES, Cauley JA, Schwartz AV, et al. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165(16043679):1612–7.PubMedCrossRef
16.
go back to reference Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(10789670):2008–12.PubMedCrossRef Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283(10789670):2008–12.PubMedCrossRef
17.
go back to reference Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions. Version 5.0.2 [updated September 2009] ed: The Cochrane Collaboration; 2009. Higgins JPT, Green S. Cochrane handbook for systematic reviews of interventions. Version 5.0.2 [updated September 2009] ed: The Cochrane Collaboration; 2009.
19.
go back to reference Al-Elq AH, Sadat-Ali M. Diabetes mellitus and male osteoporosis. Is there a relationship? Saudi Med J. 2006;27(11):1729–33.PubMed Al-Elq AH, Sadat-Ali M. Diabetes mellitus and male osteoporosis. Is there a relationship? Saudi Med J. 2006;27(11):1729–33.PubMed
20.
go back to reference Al-Maatouq MA, El-Desouki MI, Othman SA, Mattar EH, Babay ZA, Addar M. Prevalence of osteoporosis among postmenopausal females with diabetes mellitus. Saudi Med J. 2004;25(10):1423–7.PubMed Al-Maatouq MA, El-Desouki MI, Othman SA, Mattar EH, Babay ZA, Addar M. Prevalence of osteoporosis among postmenopausal females with diabetes mellitus. Saudi Med J. 2004;25(10):1423–7.PubMed
21.
go back to reference Buysschaert M, Cauwe F, Jamart J, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab. 1992;18(1):32–7.PubMed Buysschaert M, Cauwe F, Jamart J, et al. Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab. 1992;18(1):32–7.PubMed
22.
go back to reference Christensen JO, Svendsen OL. Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int. 1999;10(4):307–11.PubMedCrossRef Christensen JO, Svendsen OL. Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int. 1999;10(4):307–11.PubMedCrossRef
23.
go back to reference Cutrim DM, Pereira FA, de Paula FJ, Foss MC. Lack of relationship between glycemic control and bone mineral density in type 2 diabetes mellitus. Braz J Med Biol Res. 2007;40(2):221–7.PubMedCrossRef Cutrim DM, Pereira FA, de Paula FJ, Foss MC. Lack of relationship between glycemic control and bone mineral density in type 2 diabetes mellitus. Braz J Med Biol Res. 2007;40(2):221–7.PubMedCrossRef
24.
25.
go back to reference Hanley DA, Brown JP, Tenenhouse A, et al. Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res. 2003;18(4):784–90. doi:10.1359/jbmr.2003.18.4.784.PubMedCrossRef Hanley DA, Brown JP, Tenenhouse A, et al. Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res. 2003;18(4):784–90. doi:10.​1359/​jbmr.​2003.​18.​4.​784.PubMedCrossRef
26.
go back to reference Kwon DJ, Kim JH, Chung KW, Lee JW, Kim SP, Lee HY. Bone mineral density of the spine using dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. J Obstet Gynaecol Res. 1996;22(8697346):157–62.PubMed Kwon DJ, Kim JH, Chung KW, Lee JW, Kim SP, Lee HY. Bone mineral density of the spine using dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. J Obstet Gynaecol Res. 1996;22(8697346):157–62.PubMed
27.
go back to reference Nishitani H, Miki T, Morii H, et al. Decreased bone mineral density in diabetic patients on hemodialysis. Contrib Nephrol. 1991;90(1959351):223–7.PubMed Nishitani H, Miki T, Morii H, et al. Decreased bone mineral density in diabetic patients on hemodialysis. Contrib Nephrol. 1991;90(1959351):223–7.PubMed
28.
go back to reference Okuno Y, Nishizawa Y, Sekiya K, Hagiwara S, Miki T, Morii H. Total and regional bone mineral content in patients with non-insulin dependent diabetes mellitus. J Nutr Sci Vitaminol (Tokyo). 1991;37 Suppl(1820443):43–9. Okuno Y, Nishizawa Y, Sekiya K, Hagiwara S, Miki T, Morii H. Total and regional bone mineral content in patients with non-insulin dependent diabetes mellitus. J Nutr Sci Vitaminol (Tokyo). 1991;37 Suppl(1820443):43–9.
29.
go back to reference Yamaguchi T, Kanazawa I, Yamamoto M, et al. Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone. 2009;45(19446053):174–9.PubMedCrossRef Yamaguchi T, Kanazawa I, Yamamoto M, et al. Associations between components of the metabolic syndrome versus bone mineral density and vertebral fractures in patients with type 2 diabetes. Bone. 2009;45(19446053):174–9.PubMedCrossRef
30.
go back to reference Akin O, Gol K, Akturk M, Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol. 2003;17(12724015):19–29.PubMed Akin O, Gol K, Akturk M, Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol. 2003;17(12724015):19–29.PubMed
31.
go back to reference Hampson G, Evans C, Petitt RJ, et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia. 1998;41(9833939):1314–20.PubMedCrossRef Hampson G, Evans C, Petitt RJ, et al. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia. 1998;41(9833939):1314–20.PubMedCrossRef
32.
go back to reference Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7789645):775–82.PubMedCrossRef Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7789645):775–82.PubMedCrossRef
33.
go back to reference Oz SG, Guven GS, Kilicarslan A, Calik N, Beyazit Y, Sozen T. Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus. J Natl Med Assoc. 2006;98(17052049):1598–604.PubMed Oz SG, Guven GS, Kilicarslan A, Calik N, Beyazit Y, Sozen T. Evaluation of bone metabolism and bone mass in patients with type-2 diabetes mellitus. J Natl Med Assoc. 2006;98(17052049):1598–604.PubMed
34.
go back to reference Rishaug U, Birkeland KI, Falch JA, Vaaler S. Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest. 1995;55(7638560):257–62.PubMedCrossRef Rishaug U, Birkeland KI, Falch JA, Vaaler S. Bone mass in non-insulin-dependent diabetes mellitus. Scand J Clin Lab Invest. 1995;55(7638560):257–62.PubMedCrossRef
35.
go back to reference Sert M, Tetiker T, Kirim S, Soyupak S, Canataroglu A, Kocak M. Type 2 diabetes mellitus and osteopenia: is there an association? Acta Diabetol. 2003;40(12861410):105–8.PubMed Sert M, Tetiker T, Kirim S, Soyupak S, Canataroglu A, Kocak M. Type 2 diabetes mellitus and osteopenia: is there an association? Acta Diabetol. 2003;40(12861410):105–8.PubMed
36.
go back to reference Strotmeyer ES, Cauley JA, Schwartz AV, et al. Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: The Health, Aging, and Body Composition Study. J Bone Miner Res. 2004;19(7):1084–91. doi:10.1359/JBMR.040311.PubMedCrossRef Strotmeyer ES, Cauley JA, Schwartz AV, et al. Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: The Health, Aging, and Body Composition Study. J Bone Miner Res. 2004;19(7):1084–91. doi:10.​1359/​JBMR.​040311.PubMedCrossRef
37.
go back to reference Shan PF, Wu XP, Zhang H, et al. Bone mineral density and its relationship with body mass index in postmenopausal women with type 2 diabetes mellitus in mainland China. J Bone Miner Metab. 2009;27(2):190–7. doi:10.1007/s00774-008-0023-9.PubMedCrossRef Shan PF, Wu XP, Zhang H, et al. Bone mineral density and its relationship with body mass index in postmenopausal women with type 2 diabetes mellitus in mainland China. J Bone Miner Metab. 2009;27(2):190–7. doi:10.​1007/​s00774-008-0023-9.PubMedCrossRef
38.
go back to reference Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif Tissue Int. 2007;80(6):353–8. doi:10.1007/s00223-007-9003-7.PubMedCrossRef Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif Tissue Int. 2007;80(6):353–8. doi:10.​1007/​s00223-007-9003-7.PubMedCrossRef
39.
go back to reference Schneider S, Schmitt G, Mau H, Schmitt H, Sabo D, Richter W. Prevalence and correlates of osteoarthritis in Germany. Representative data from the First National Health Survey. Orthopade. 2005;34(15912329):782–90.PubMedCrossRef Schneider S, Schmitt G, Mau H, Schmitt H, Sabo D, Richter W. Prevalence and correlates of osteoarthritis in Germany. Representative data from the First National Health Survey. Orthopade. 2005;34(15912329):782–90.PubMedCrossRef
40.
go back to reference Isaia G, Bodrato L, Carlevatto V, Mussetta M, Salamano G, Molinatti GM. Osteoporosis in type II diabetes. Acta Diabetol Lat. 1987;24(3439401):305–10.PubMedCrossRef Isaia G, Bodrato L, Carlevatto V, Mussetta M, Salamano G, Molinatti GM. Osteoporosis in type II diabetes. Acta Diabetol Lat. 1987;24(3439401):305–10.PubMedCrossRef
41.
go back to reference Buday B, Horvath T, Kulcsar E, et al. Effect of progressive insulin resistance on the correlation of glucose metabolism and bone status. Orv Hetil. 2007;148(17561482):1127–33.PubMedCrossRef Buday B, Horvath T, Kulcsar E, et al. Effect of progressive insulin resistance on the correlation of glucose metabolism and bone status. Orv Hetil. 2007;148(17561482):1127–33.PubMedCrossRef
42.
go back to reference Horiuchi T, Nakamura T, Miyao M, et al. Bone mineral density in postmenopausal elderly women with type 2 diabetes. Nippon Ronen Igakkai Zasshi. 1995;32(8598632):756–60.PubMedCrossRef Horiuchi T, Nakamura T, Miyao M, et al. Bone mineral density in postmenopausal elderly women with type 2 diabetes. Nippon Ronen Igakkai Zasshi. 1995;32(8598632):756–60.PubMedCrossRef
43.
go back to reference Komatsu Y, Majima T. Negative correlation between BMD and HbA1C in patients with type 2 diabetes. Clin Calcium. 2006;16(16883041):1327–31.PubMed Komatsu Y, Majima T. Negative correlation between BMD and HbA1C in patients with type 2 diabetes. Clin Calcium. 2006;16(16883041):1327–31.PubMed
44.
go back to reference Sahin G, Bagis S, Cimen OB, Ozisik S, Guler H, Erdogan C. Lumbar and femoral bone mineral density in type 2 Turkish diabetic patients. Acta Medica (Hradec Kralove). 2001;44(4):141–3. Sahin G, Bagis S, Cimen OB, Ozisik S, Guler H, Erdogan C. Lumbar and femoral bone mineral density in type 2 Turkish diabetic patients. Acta Medica (Hradec Kralove). 2001;44(4):141–3.
45.
go back to reference Bonds DE, Larson JC, Schwartz AV, et al. Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J Clin Endocrinol Metab. 2006;91(16804043):3404–10.PubMedCrossRef Bonds DE, Larson JC, Schwartz AV, et al. Risk of fracture in women with type 2 diabetes: the Women’s Health Initiative Observational Study. J Clin Endocrinol Metab. 2006;91(16804043):3404–10.PubMedCrossRef
46.
go back to reference Perez-Castrillon J-L, De Luis D, Martin-Escudero JC, Asensio T, del Amo R, Izaola O. Non-insulin-dependent diabetes, bone mineral density, and cardiovascular risk factors. J Diabetes Complications. 2004;18(15531180):317–21.PubMedCrossRef Perez-Castrillon J-L, De Luis D, Martin-Escudero JC, Asensio T, del Amo R, Izaola O. Non-insulin-dependent diabetes, bone mineral density, and cardiovascular risk factors. J Diabetes Complications. 2004;18(15531180):317–21.PubMedCrossRef
47.
go back to reference Sosa M, Dominguez M, Navarro MC, et al. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications. 1996;10(8835919):201–5.PubMedCrossRef Sosa M, Dominguez M, Navarro MC, et al. Bone mineral metabolism is normal in non-insulin-dependent diabetes mellitus. J Diabetes Complications. 1996;10(8835919):201–5.PubMedCrossRef
48.
go back to reference Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22(7):1196–200.PubMedCrossRef Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22(7):1196–200.PubMedCrossRef
49.
go back to reference Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DIW, Cooper C. Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia. 2004;47(15565368):1963–8. Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DIW, Cooper C. Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia. 2004;47(15565368):1963–8.
50.
go back to reference Bridges MJ, Moochhala SH, Barbour J, Kelly CA. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol. 2005;42(15944841):82–6.PubMedCrossRef Bridges MJ, Moochhala SH, Barbour J, Kelly CA. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol. 2005;42(15944841):82–6.PubMedCrossRef
52.
go back to reference Rakic V, Davis WA, Chubb SAP, Islam FMA, Prince RL, Davis TME. Bone mineral density and its determinants in diabetes: the Fremantle Diabetes Study. Diabetologia. 2006;49(16518589):863–71.PubMedCrossRef Rakic V, Davis WA, Chubb SAP, Islam FMA, Prince RL, Davis TME. Bone mineral density and its determinants in diabetes: the Fremantle Diabetes Study. Diabetologia. 2006;49(16518589):863–71.PubMedCrossRef
53.
go back to reference Hadzibegovic I, Miskic B, Cosic V, Prvulovic D, Bistrovic D. Increased bone mineral density in postmenopausal women with type 2 diabetes mellitus. Ann Saudi Med. 2008;28(18398285):102–4.PubMedCrossRef Hadzibegovic I, Miskic B, Cosic V, Prvulovic D, Bistrovic D. Increased bone mineral density in postmenopausal women with type 2 diabetes mellitus. Ann Saudi Med. 2008;28(18398285):102–4.PubMedCrossRef
54.
go back to reference Anaforoglu I, Nar-Demirer A, Bascil-Tutuncu N, Ertorer ME. Prevalence of osteoporosis and factors affecting bone mineral density among postmenopausal Turkish women with type 2 diabetes. J Diabetes Complications. 2009;23(18413190):12–7.PubMedCrossRef Anaforoglu I, Nar-Demirer A, Bascil-Tutuncu N, Ertorer ME. Prevalence of osteoporosis and factors affecting bone mineral density among postmenopausal Turkish women with type 2 diabetes. J Diabetes Complications. 2009;23(18413190):12–7.PubMedCrossRef
55.
go back to reference Shan PF, Wu XP, Zhang H, Cao XZ, Yuan LQ, Liao EY. Age-related bone mineral density, osteoporosis rate and risk of vertebral fracture in mainland Chinese women with type 2 diabetes mellitus. J Endocrinol Invest. 2011;34(3):190–6. doi:10.3275/7239.PubMed Shan PF, Wu XP, Zhang H, Cao XZ, Yuan LQ, Liao EY. Age-related bone mineral density, osteoporosis rate and risk of vertebral fracture in mainland Chinese women with type 2 diabetes mellitus. J Endocrinol Invest. 2011;34(3):190–6. doi:10.​3275/​7239.PubMed
57.
go back to reference Javed F, Yu W, Thornton J, Colt E. Effect of fat on measurement of bone mineral density. Int J Body Compos Res. 2009;7(1):37–40.PubMed Javed F, Yu W, Thornton J, Colt E. Effect of fat on measurement of bone mineral density. Int J Body Compos Res. 2009;7(1):37–40.PubMed
58.
go back to reference Evans EM, Mojtahedi MC, Kessinger RB, Misic MM. Simulated change in body fatness affects Hologic QDR 4500A whole body and central DXA bone measures. J Clin Densitom. 2006;9(16931350):315–22.PubMedCrossRef Evans EM, Mojtahedi MC, Kessinger RB, Misic MM. Simulated change in body fatness affects Hologic QDR 4500A whole body and central DXA bone measures. J Clin Densitom. 2006;9(16931350):315–22.PubMedCrossRef
60.
go back to reference Kanabrocki EL, Hermida RC, Wright M, et al. Circadian variation of serum leptin in healthy and diabetic men. Chronobiol Int. 2001;18(2):273–83.PubMedCrossRef Kanabrocki EL, Hermida RC, Wright M, et al. Circadian variation of serum leptin in healthy and diabetic men. Chronobiol Int. 2001;18(2):273–83.PubMedCrossRef
61.
go back to reference Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, Baile CA. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res. 2005;20(6):994–1001. doi:10.1359/JBMR.050103.PubMedCrossRef Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, Baile CA. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res. 2005;20(6):994–1001. doi:10.​1359/​JBMR.​050103.PubMedCrossRef
62.
go back to reference Steppan CM, Crawford DT, Chidsey-Frink KL, Ke H, Swick AG. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept. 2000;92(1–3):73–8.PubMedCrossRef Steppan CM, Crawford DT, Chidsey-Frink KL, Ke H, Swick AG. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept. 2000;92(1–3):73–8.PubMedCrossRef
63.
go back to reference Gordeladze JO, Drevon CA, Syversen U, Reseland JE. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85(11968022):825–36.PubMedCrossRef Gordeladze JO, Drevon CA, Syversen U, Reseland JE. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85(11968022):825–36.PubMedCrossRef
64.
go back to reference Cornish J, Callon KE, Bava U, et al. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol. 2002;175(12429038):405–15.PubMedCrossRef Cornish J, Callon KE, Bava U, et al. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol. 2002;175(12429038):405–15.PubMedCrossRef
65.
go back to reference Holloway WR, Collier FM, Aitken CJ, et al. Leptin inhibits osteoclast generation. J Bone Miner Res. 2002;17(11811550):200–9.PubMedCrossRef Holloway WR, Collier FM, Aitken CJ, et al. Leptin inhibits osteoclast generation. J Bone Miner Res. 2002;17(11811550):200–9.PubMedCrossRef
66.
go back to reference Berner HS, Lyngstadaas SP, Spahr A, et al. Adiponectin and its receptors are expressed in bone-forming cells. Bone. 2004;35(15454091):842–9.PubMedCrossRef Berner HS, Lyngstadaas SP, Spahr A, et al. Adiponectin and its receptors are expressed in bone-forming cells. Bone. 2004;35(15454091):842–9.PubMedCrossRef
67.
go back to reference Thommesen L, Stunes AK, Monjo M, et al. Expression and regulation of resistin in osteoblasts and osteoclasts indicate a role in bone metabolism. J Cell Biochem. 2006;99(16721825):824–34.PubMedCrossRef Thommesen L, Stunes AK, Monjo M, et al. Expression and regulation of resistin in osteoblasts and osteoclasts indicate a role in bone metabolism. J Cell Biochem. 2006;99(16721825):824–34.PubMedCrossRef
69.
70.
go back to reference Oshima K, Nampei A, Matsuda M, et al. Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun. 2005;331(15850790):520–6.PubMedCrossRef Oshima K, Nampei A, Matsuda M, et al. Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun. 2005;331(15850790):520–6.PubMedCrossRef
71.
72.
go back to reference Gómez-Ambrosi J, Frühbeck G. Evidence for the involvement of resistin in inflammation and cardiovascular disease. Curr Diabetes Rev. 2005;1:227–34.PubMedCrossRef Gómez-Ambrosi J, Frühbeck G. Evidence for the involvement of resistin in inflammation and cardiovascular disease. Curr Diabetes Rev. 2005;1:227–34.PubMedCrossRef
74.
go back to reference Pun KK, Lau P, Ho PW. The characterization, regulation, and function of insulin receptors on osteoblast-like clonal osteosarcoma cell line. J Bone Miner Res. 1989;4(2692404):853–62.PubMed Pun KK, Lau P, Ho PW. The characterization, regulation, and function of insulin receptors on osteoblast-like clonal osteosarcoma cell line. J Bone Miner Res. 1989;4(2692404):853–62.PubMed
76.
go back to reference Langlois JA, Rosen CJ, Visser M, et al. Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J Clin Endocrinol Metab. 1998;83(12):4257–62.PubMedCrossRef Langlois JA, Rosen CJ, Visser M, et al. Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J Clin Endocrinol Metab. 1998;83(12):4257–62.PubMedCrossRef
77.
go back to reference Zhao G, Monier-Faugere MC, Langub MC, et al. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology. 2000;141(10875273):2674–82.PubMedCrossRef Zhao G, Monier-Faugere MC, Langub MC, et al. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology. 2000;141(10875273):2674–82.PubMedCrossRef
79.
go back to reference Schoofs MW, van der Klift M, Hofman A, et al. Thiazide diuretics and the risk for hip fracture. Ann Intern Med. 2003;139(6):476–82.PubMed Schoofs MW, van der Klift M, Hofman A, et al. Thiazide diuretics and the risk for hip fracture. Ann Intern Med. 2003;139(6):476–82.PubMed
80.
go back to reference Pasco JA, Kotowicz MA, Henry MJ, Sanders KM, Nicholson GC. Statin use, bone mineral density, and fracture risk: Geelong Osteoporosis Study. Arch Intern Med. 2002;162(5):537–40.PubMedCrossRef Pasco JA, Kotowicz MA, Henry MJ, Sanders KM, Nicholson GC. Statin use, bone mineral density, and fracture risk: Geelong Osteoporosis Study. Arch Intern Med. 2002;162(5):537–40.PubMedCrossRef
81.
82.
go back to reference Schurman L, McCarthy AD, Sedlinsky C, et al. Metformin reverts deleterious effects of advanced glycation end-products (AGEs) on osteoblastic cells. Exp Clin Endocrinol Diabetes. 2008;116(6):333–40. doi:10.1055/s-2007-992786.PubMedCrossRef Schurman L, McCarthy AD, Sedlinsky C, et al. Metformin reverts deleterious effects of advanced glycation end-products (AGEs) on osteoblastic cells. Exp Clin Endocrinol Diabetes. 2008;116(6):333–40. doi:10.​1055/​s-2007-992786.PubMedCrossRef
84.
go back to reference Burghardt AJ, Issever AS, Schwartz AV, et al. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95(11):5045–55. doi:10.1210/jc.2010-0226.PubMedCrossRef Burghardt AJ, Issever AS, Schwartz AV, et al. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95(11):5045–55. doi:10.​1210/​jc.​2010-0226.PubMedCrossRef
85.
go back to reference Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(15919781):1615–25.PubMedCrossRef Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(15919781):1615–25.PubMedCrossRef
86.
go back to reference Yamaguchi T, Sugimoto T. Bone metabolism and fracture risk in type 2 diabetes mellitus [review]. Endocr J. 2011;58(8):613–24.PubMedCrossRef Yamaguchi T, Sugimoto T. Bone metabolism and fracture risk in type 2 diabetes mellitus [review]. Endocr J. 2011;58(8):613–24.PubMedCrossRef
87.
go back to reference Evans WJ, Campbell WW. Sarcopenia and age-related changes in body composition and functional capacity. J Nutr. 1993;123(2 Suppl):465–8.PubMed Evans WJ, Campbell WW. Sarcopenia and age-related changes in body composition and functional capacity. J Nutr. 1993;123(2 Suppl):465–8.PubMed
89.
go back to reference Giangregorio LM, Leslie WD, Lix LM, et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res. 2011;. doi:10.1002/jbmr.556. Giangregorio LM, Leslie WD, Lix LM, et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res. 2011;. doi:10.​1002/​jbmr.​556.
90.
go back to reference Hippisley-Cox J, Coupland C. Predicting risk of osteoporotic fracture in men and women in England and Wales: prospective derivation and validation of QFractureScores. BMJ. 2009;339:b4229. doi:10.1136/bmj.b4229.PubMedCrossRef Hippisley-Cox J, Coupland C. Predicting risk of osteoporotic fracture in men and women in England and Wales: prospective derivation and validation of QFractureScores. BMJ. 2009;339:b4229. doi:10.​1136/​bmj.​b4229.PubMedCrossRef
Metadata
Title
Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies
Authors
Lili Ma
Ling Oei
Lindi Jiang
Karol Estrada
Huiyong Chen
Zhen Wang
Qiang Yu
Maria Carola Zillikens
Xin Gao
Fernando Rivadeneira
Publication date
01-05-2012
Publisher
Springer Netherlands
Published in
European Journal of Epidemiology / Issue 5/2012
Print ISSN: 0393-2990
Electronic ISSN: 1573-7284
DOI
https://doi.org/10.1007/s10654-012-9674-x

Other articles of this Issue 5/2012

European Journal of Epidemiology 5/2012 Go to the issue