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Published in: Osteoporosis International 2/2012

01-02-2012 | Original Article

Bone structure and turnover in type 2 diabetes mellitus

Authors: A. Shu, M. T. Yin, E. Stein, S. Cremers, E. Dworakowski, R. Ives, M. R. Rubin

Published in: Osteoporosis International | Issue 2/2012

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Abstract

Summary

We compared skeletal parameters in type 2 diabetic (T2DM) and non-diabetic postmenopausal women. Bone structure by dual energy x-ray absorptiometry (DXA) and HR-pQCT was not different, although procollagen type 1 amino-terminal propeptide (P1NP) and osteocalcin levels were lower in T2DM.

Introduction

T2DM is associated with increased fracture risk, but, paradoxically, with higher cross-sectional bone density (BMD) as measured by DXA. We sought explanations to this puzzle by investigating detailed structural and biochemical skeletal parameters in T2DM.

Methods

Cross-sectional comparison of 25 postmenopausal T2DM women and 25 matched controls using DXA, high-resolution peripheral quantitative computed tomography (HR-pQCT) and biochemical bone turnover markers.

Results

BMD by DXA did not differ between T2DM and controls. HR-pQCT assessment also did not differ, with the exception of cortical area at the tibia, which tended to be lower in the diabetics (difference of 12 ± 6 [mean ± SD] mm, p = 0.06). P1NP and osteocalcin levels were lower in T2DM as compared to controls (P1NP, 34.3 ± 16 vs. 57.3 ± 28 ng/ml; p = 0.005; osteocalcin, 4.5 ± 2 vs. 6.2 ± 2 nmol/L; p = 0.001).

Conclusions

Postmenopausal women with T2DM had lower levels of bone formation markers as compared to controls. Aside from a possible decrease in cortical bone area at a weight-bearing site, bone structure was not altered in T2DM. Lower bone turnover may be a skeletal parameter that is present in T2DM.
Literature
1.
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 18:784–790PubMedCrossRef 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 18:784–790PubMedCrossRef
2.
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 19:1084–1091PubMedCrossRef 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 19:1084–1091PubMedCrossRef
3.
go back to reference Bonds DE, Larson JC, Schwartz AV et al (2006) Risk of fracture in women with type 2 diabetes: the women's health initiative observational study. J Clin Endocrinol Metab 91:3404–3410PubMedCrossRef Bonds DE, Larson JC, Schwartz AV et al (2006) Risk of fracture in women with type 2 diabetes: the women's health initiative observational study. J Clin Endocrinol Metab 91:3404–3410PubMedCrossRef
4.
go back to reference Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int 18:427–444PubMedCrossRef Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos Int 18:427–444PubMedCrossRef
5.
go back to reference Lipscombe LL, Jamal SA, Booth GL, Hawker GA (2007) The risk of hip fractures in older individuals with diabetes: a population-based study. Diab Care 30:835–841CrossRef Lipscombe LL, Jamal SA, Booth GL, Hawker GA (2007) The risk of hip fractures in older individuals with diabetes: a population-based study. Diab Care 30:835–841CrossRef
6.
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 165:1612–1617PubMedCrossRef 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 165:1612–1617PubMedCrossRef
7.
go back to reference Janghorbani M, Feskanich D, Willett WC, Hu F (2006) Prospective study of diabetes and risk of hip fracture: the Nurses' Health Study. Diab Care 29:1573–1578CrossRef Janghorbani M, Feskanich D, Willett WC, Hu F (2006) Prospective study of diabetes and risk of hip fracture: the Nurses' Health Study. Diab Care 29:1573–1578CrossRef
8.
go back to reference Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2009) Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res 24:702–709PubMedCrossRef Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2009) Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J Bone Miner Res 24:702–709PubMedCrossRef
9.
go back to reference Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55PubMedCrossRef Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55PubMedCrossRef
10.
11.
go back to reference Melton LJ 3rd, Riggs BL, Leibson CL et al (2008) A bone structural basis for fracture risk in diabetes. J Clin Endocrinol Metab 93:4804–4809PubMedCrossRef Melton LJ 3rd, Riggs BL, Leibson CL et al (2008) A bone structural basis for fracture risk in diabetes. J Clin Endocrinol Metab 93:4804–4809PubMedCrossRef
12.
go back to reference Fulzele K, Riddle RC, DiGirolamo DJ et al (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142:309–319PubMedCrossRef Fulzele K, Riddle RC, DiGirolamo DJ et al (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142:309–319PubMedCrossRef
13.
go back to reference Petit MA, Paudel ML, Taylor BC et al (2010) Bone mass and strength in older men with type 2 diabetes: The osteoporotic fractures in men study. J Bone Miner Res 25:285–291PubMedCrossRef Petit MA, Paudel ML, Taylor BC et al (2010) Bone mass and strength in older men with type 2 diabetes: The osteoporotic fractures in men study. J Bone Miner Res 25:285–291PubMedCrossRef
14.
go back to reference Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512PubMedCrossRef Gerdhem P, Isaksson A, Akesson K, Obrant KJ (2005) Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506–1512PubMedCrossRef
15.
go back to reference Kanazawa I, Yamaguchi T, Yamamoto M et al (2009) Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:45–49PubMedCrossRef Kanazawa I, Yamaguchi T, Yamamoto M et al (2009) Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:45–49PubMedCrossRef
16.
go back to reference Sayinalp S, Gedik O, Koray Z (1995) Increasing serum osteocalcin after glycemic control in diabetic men. Calcif Tissue Int 57:422–425PubMedCrossRef Sayinalp S, Gedik O, Koray Z (1995) Increasing serum osteocalcin after glycemic control in diabetic men. Calcif Tissue Int 57:422–425PubMedCrossRef
17.
go back to reference Rosato MT, Schneider SH, Shapses SA (1998) Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int 63:107–111PubMedCrossRef Rosato MT, Schneider SH, Shapses SA (1998) Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int 63:107–111PubMedCrossRef
18.
go back to reference Dobnig H, Piswanger-Solkner JC, Roth M et al (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363PubMedCrossRef Dobnig H, Piswanger-Solkner JC, Roth M et al (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363PubMedCrossRef
19.
go back to reference Okazaki R, Totsuka Y, Hamano K et al (1997) Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 82:2915–2920PubMedCrossRef Okazaki R, Totsuka Y, Hamano K et al (1997) Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 82:2915–2920PubMedCrossRef
20.
go back to reference Cohen A, Liu XS, Stein EM et al (2009) Bone microarchitecture and stiffness in premenopausal women with idiopathic osteoporosis. J Clin Endocrinol Metab 94:4351–4360PubMedCrossRef Cohen A, Liu XS, Stein EM et al (2009) Bone microarchitecture and stiffness in premenopausal women with idiopathic osteoporosis. J Clin Endocrinol Metab 94:4351–4360PubMedCrossRef
21.
go back to reference Walker MD, McMahon DJ, Udesky J, Liu G, Bilezikian JP (2009) Application of high-resolution skeletal imaging to measurements of volumetric BMD and skeletal microarchitecture in Chinese-American and white women: explanation of a paradox. J Bone Miner Res 24:1953–1959PubMedCrossRef Walker MD, McMahon DJ, Udesky J, Liu G, Bilezikian JP (2009) Application of high-resolution skeletal imaging to measurements of volumetric BMD and skeletal microarchitecture in Chinese-American and white women: explanation of a paradox. J Bone Miner Res 24:1953–1959PubMedCrossRef
22.
go back to reference Cohen A, Dempster DW, Muller R et al (2010) Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos Int 21(2):263–273PubMedCrossRef Cohen A, Dempster DW, Muller R et al (2010) Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos Int 21(2):263–273PubMedCrossRef
23.
go back to reference Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515PubMedCrossRef Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515PubMedCrossRef
24.
go back to reference Gomez B Jr, Ardakani S, Ju J et al (1995) Monoclonal antibody assay for measuring bone-specific alkaline phosphatase activity in serum. Clin Chem 41:1560–1566PubMed Gomez B Jr, Ardakani S, Ju J et al (1995) Monoclonal antibody assay for measuring bone-specific alkaline phosphatase activity in serum. Clin Chem 41:1560–1566PubMed
25.
go back to reference Rosenquist C, Qvist P, Bjarnason N, Christiansen C (1995) Measurement of a more stable region of osteocalcin in serum by ELISA with two monoclonal antibodies. Clin Chem 41:1439–1445PubMed Rosenquist C, Qvist P, Bjarnason N, Christiansen C (1995) Measurement of a more stable region of osteocalcin in serum by ELISA with two monoclonal antibodies. Clin Chem 41:1439–1445PubMed
26.
go back to reference Clowes JA, Allen HC, Prentis DM, Eastell R, Blumsohn A (2003) Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab 88:4867–4873PubMedCrossRef Clowes JA, Allen HC, Prentis DM, Eastell R, Blumsohn A (2003) Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab 88:4867–4873PubMedCrossRef
27.
go back to reference Inaba M, Nishizawa Y, Mita K et al (1999) Poor glycemic control impairs the response of biochemical parameters of bone formation and resorption to exogenous 1,25-dihydroxyvitamin D3 in patients with type 2 diabetes. Osteoporos Int 9:525–531PubMedCrossRef Inaba M, Nishizawa Y, Mita K et al (1999) Poor glycemic control impairs the response of biochemical parameters of bone formation and resorption to exogenous 1,25-dihydroxyvitamin D3 in patients with type 2 diabetes. Osteoporos Int 9:525–531PubMedCrossRef
28.
go back to reference Inaba M, Terada M, Koyama H et al (1995) Influence of high glucose on 1,25-dihydroxyvitamin D3-induced effect on human osteoblast-like MG-63 cells. J Bone Miner Res 10:1050–1056PubMedCrossRef Inaba M, Terada M, Koyama H et al (1995) Influence of high glucose on 1,25-dihydroxyvitamin D3-induced effect on human osteoblast-like MG-63 cells. J Bone Miner Res 10:1050–1056PubMedCrossRef
29.
go back to reference Terada M, Inaba M, Yano Y et al (1998) Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone 22:17–23PubMedCrossRef Terada M, Inaba M, Yano Y et al (1998) Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone 22:17–23PubMedCrossRef
30.
go back to reference Zinman B, Haffner SM, Herman WH et al (2010) Effect of rosiglitazone, metformin, and glyburide on bone biomarkers in patients with type 2 diabetes. J Clin Endocrinol Metab 95:134–142PubMedCrossRef Zinman B, Haffner SM, Herman WH et al (2010) Effect of rosiglitazone, metformin, and glyburide on bone biomarkers in patients with type 2 diabetes. J Clin Endocrinol Metab 95:134–142PubMedCrossRef
31.
go back to reference Kindblom JM, Ohlsson C, Ljunggren O et al (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785–791PubMedCrossRef Kindblom JM, Ohlsson C, Ljunggren O et al (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785–791PubMedCrossRef
32.
go back to reference Eastell R, Delmas PD, Hodgson SF, Eriksen EF, Mann KG, Riggs BL (1988) Bone formation rate in older normal women: concurrent assessment with bone histomorphometry, calcium kinetics, and biochemical markers. J Clin Endocrinol Metab 67:741–748PubMedCrossRef Eastell R, Delmas PD, Hodgson SF, Eriksen EF, Mann KG, Riggs BL (1988) Bone formation rate in older normal women: concurrent assessment with bone histomorphometry, calcium kinetics, and biochemical markers. J Clin Endocrinol Metab 67:741–748PubMedCrossRef
33.
go back to reference Vico L, Zouch M, Amirouche A et al (2008) High-resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res 23:1741–1750PubMedCrossRef Vico L, Zouch M, Amirouche A et al (2008) High-resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res 23:1741–1750PubMedCrossRef
34.
go back to reference Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD (2007) Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res 22:425–433PubMedCrossRef Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD (2007) Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res 22:425–433PubMedCrossRef
35.
go back to reference Ferron M, Wei J, Yoshizawa T et al (2010) Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142:296–308PubMedCrossRef Ferron M, Wei J, Yoshizawa T et al (2010) Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142:296–308PubMedCrossRef
36.
go back to reference Petit MA, Paudel ML, Taylor BC et al (2010) Bone Mass and Strength in Older Men with Type 2 Diabetes: The osteoporotic fractures in men study. J Bone Miner Res 25(2):285–291PubMedCrossRef Petit MA, Paudel ML, Taylor BC et al (2010) Bone Mass and Strength in Older Men with Type 2 Diabetes: The osteoporotic fractures in men study. J Bone Miner Res 25(2):285–291PubMedCrossRef
37.
go back to reference Kazakia GJ, Hyun B, Burghardt AJ et al (2008) In vivo determination of bone structure in postmenopausal women: a comparison of HR-pQCT and high-field MR imaging. J Bone Miner Res 23:463–474PubMedCrossRef Kazakia GJ, Hyun B, Burghardt AJ et al (2008) In vivo determination of bone structure in postmenopausal women: a comparison of HR-pQCT and high-field MR imaging. J Bone Miner Res 23:463–474PubMedCrossRef
38.
go back to reference Paul RG, Bailey AJ (1996) Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 28:1297–1310PubMedCrossRef Paul RG, Bailey AJ (1996) Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 28:1297–1310PubMedCrossRef
39.
go back to reference Schwartz AV, Garnero P, Hillier TA et al (2009) Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 94:2380–2386PubMedCrossRef Schwartz AV, Garnero P, Hillier TA et al (2009) Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 94:2380–2386PubMedCrossRef
40.
go back to reference Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T (2008) Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 93:1013–1019PubMedCrossRef Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T (2008) Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab 93:1013–1019PubMedCrossRef
41.
go back to reference Stein EM, Liu XS, Nickolas TL et al (2010) Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res 25:2296–2305CrossRef Stein EM, Liu XS, Nickolas TL et al (2010) Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res 25:2296–2305CrossRef
Metadata
Title
Bone structure and turnover in type 2 diabetes mellitus
Authors
A. Shu
M. T. Yin
E. Stein
S. Cremers
E. Dworakowski
R. Ives
M. R. Rubin
Publication date
01-02-2012
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 2/2012
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-011-1595-0

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