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Published in: Journal of Diabetes & Metabolic Disorders 1/2019

01-06-2019 | Osteoporosis | Research Article

Effect of diabetes on BMD and TBS values as determinants of bone health in the elderly: Bushehr Elderly Health program

Authors: Mahbube Ebrahimpur, Farshad Sharifi, Farzaneh Amini Nezhad, Mohammad Bagherzadeh, Afshin Ostovar, Gita Shafiee, Ramin Heshmat, Neda Mehrdad, Faride Razi, Patricia Khashayar, Iraj Nabipour, Bagher Larijani

Published in: Journal of Diabetes & Metabolic Disorders | Issue 1/2019

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Abstract

Background

Considering the aging population associated with higher osteoporotic fracture risk, high prevalence of diabetes and its effect on bone health along with lack of information on bone quality using common methods (BMD) the aim of present study was to determine the association between trabecular bone score (TBS) and diabetes in an elderly population participating in Bushehr Elderly Health (BEH) program.

Materials and methods

This cross-sectional study was performed on data collected during the BEH Program, stage II. Anthropometric indices were measured based on NHANES III protocol. Diabetes and pre-diabetes were defined according to ADA Guideline 2018. Bone density was measured using DXA method (DXA, Discovery WI, Hologic Inc., USA). A software installed on the same device (TBS iNsight® software) was applied to assess TBS values. Variables related to bone health were compared based on their glycemic status (participants with diabetes, participants with prediabetes, and normoglycemic) using analysis of variance. Univariate and multivariate linear and logistic regression models were used to determine the association between TBS values and bone density in different glycemic states.

Results

The data of 2263 participant aged 60 years and over were analyzed. Mean TBS values were significantly different between participants with diabetes, participants with prediabetes, and normoglycemic groups (P = 0.004;, however, P trend was not significant (0.400)). Mean BMD values at femoral neck and lumbar spine were significantly higher in diabetics compared with those diagnosed with pre-diabetes; the latter also had higher bone density compared with normoglycemic individuals (both P ANOVA test and P trends for means were < 0.01]. In univariate linear regression model, TBS values were negatively associated with pre-diabetes (β = −0.070; P < 0.001) but not with diabetes (β = −0.002, P = 0.915). This significant relationship disappeared when the results were adjusted for BMI. In fully adjusted multivariate logistic regression models, odds ratio linking pre-diabetes and diabetes with spinal osteoporosis was 0.861 (CI 95% 0.670–1.105) and 0.525 (CI 95% 0.392–0.701), respectively. As for femoral osteoporosis, odds ratio was 0.615 (CI 95% 0.407–0.928) and 0.968 (CI 95% 0.629–1.489), correspondingly. Moreover, for cumulative osteoporosis, the odds were 0.843 (CI 95% 0.676–1.106) and 0.551 (CI 95% 0.415–0.732), respectively.

Conclusion

Our findings suggest that subjects with pre-diabetes and diabetes have higher bone mineral density than normoglycemic subjects; the quality of bone, however, was not different between them. The discordance between BMD and TBS values in participants with diabetes suggest that although these patients have higher BMD values, their quality of bone microarchitecture may not be better than normoglycemic subjects.
Footnotes
1
Homeostatic model assessment- Insulin resistance
 
Literature
1.
go back to reference Schwartz AV, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(1):32–8.CrossRefPubMed Schwartz AV, et al. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(1):32–8.CrossRefPubMed
2.
go back to reference Strotmeyer ES, 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.CrossRefPubMed Strotmeyer ES, 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.CrossRefPubMed
3.
go back to reference Bonds DE, et al. Risk of fracture in women with type 2 diabetes: the Women’s health initiative observational study. J Clin Endocrinol Metab. 2006;91(9):3404–10.CrossRefPubMed Bonds DE, et al. Risk of fracture in women with type 2 diabetes: the Women’s health initiative observational study. J Clin Endocrinol Metab. 2006;91(9):3404–10.CrossRefPubMed
5.
go back to reference Hanley D, 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.CrossRefPubMed Hanley D, 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.CrossRefPubMed
6.
go back to reference Barrett-Connor E, Kritz-Silverstein D. Does hyperinsulinemia preserve bone? Diabetes Care. 1996;19(12):1388–92.CrossRefPubMed Barrett-Connor E, Kritz-Silverstein D. Does hyperinsulinemia preserve bone? Diabetes Care. 1996;19(12):1388–92.CrossRefPubMed
7.
go back to reference Janghorbani M, et al. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505.CrossRefPubMed Janghorbani M, et al. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495–505.CrossRefPubMed
8.
go back to reference Yaturu S, et al. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2008;15(1):CR5–9. Yaturu S, et al. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2008;15(1):CR5–9.
9.
go back to reference Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24(7):1192–7.CrossRefPubMed Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24(7):1192–7.CrossRefPubMed
10.
12.
go back to reference Shafiee G, et al. Bushehr Elderly Health (BEH) programme: study protocol and design of musculoskeletal system and cognitive function (stage II). BMJ Open. 2017;7(8):e013606.CrossRefPubMedPubMedCentral Shafiee G, et al. Bushehr Elderly Health (BEH) programme: study protocol and design of musculoskeletal system and cognitive function (stage II). BMJ Open. 2017;7(8):e013606.CrossRefPubMedPubMedCentral
13.
go back to reference Ervin RB. Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States. National Health Statistics Reports. 2009;13:1–8. Ervin RB. Prevalence of metabolic syndrome among adults 20 years of age and over, by sex, age, race and ethnicity, and body mass index: United States. National Health Statistics Reports. 2009;13:1–8.
14.
go back to reference Association, A.D. 2. Classification and diagnosis of diabetes. Diabetes Care. 2017;40(Supplement 1):S11–24.CrossRef Association, A.D. 2. Classification and diagnosis of diabetes. Diabetes Care. 2017;40(Supplement 1):S11–24.CrossRef
15.
go back to reference Yamaguchi T, 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(2):174–9.CrossRefPubMed Yamaguchi T, 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(2):174–9.CrossRefPubMed
16.
go back to reference Kinjo M, Setoguchi S, Solomon DH. Bone mineral density in adults with the metabolic syndrome: analysis in a population-based US sample. J Clin Endocrinol Metab. 2007;92(11):4161–4.CrossRefPubMed Kinjo M, Setoguchi S, Solomon DH. Bone mineral density in adults with the metabolic syndrome: analysis in a population-based US sample. J Clin Endocrinol Metab. 2007;92(11):4161–4.CrossRefPubMed
17.
go back to reference Holmberg AH, et al. The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women. J Clin Endocrinol Metab. 2008;93(3):815–22.CrossRefPubMed Holmberg AH, et al. The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women. J Clin Endocrinol Metab. 2008;93(3):815–22.CrossRefPubMed
18.
go back to reference Von Muhlen D, et al. Associations between the metabolic syndrome and bone health in older men and women: the rancho Bernardo study. Osteoporos Int. 2007;18(10):1337–44.CrossRef Von Muhlen D, et al. Associations between the metabolic syndrome and bone health in older men and women: the rancho Bernardo study. Osteoporos Int. 2007;18(10):1337–44.CrossRef
19.
go back to reference Muka T, et al. The association between metabolic syndrome, bone mineral density, hip bone geometry and fracture risk: the Rotterdam study. PLoS One. 2015;10(6):e0129116.CrossRefPubMedPubMedCentral Muka T, et al. The association between metabolic syndrome, bone mineral density, hip bone geometry and fracture risk: the Rotterdam study. PLoS One. 2015;10(6):e0129116.CrossRefPubMedPubMedCentral
20.
go back to reference Oei L, et al. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam study. Diabetes Care. 2013;36(6):1619–28.CrossRefPubMedPubMedCentral Oei L, et al. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam study. Diabetes Care. 2013;36(6):1619–28.CrossRefPubMedPubMedCentral
21.
go back to reference Leslie WD, et al. TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab. 2013;98(2):602–9.CrossRefPubMed Leslie WD, et al. TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab. 2013;98(2):602–9.CrossRefPubMed
22.
go back to reference Dhaliwal R, et al. Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int. 2014;25(7):1969–73.CrossRefPubMed Dhaliwal R, et al. Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int. 2014;25(7):1969–73.CrossRefPubMed
23.
go back to reference Kim JH, et al. Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab. 2015;100(2):475–82.CrossRefPubMed Kim JH, et al. Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab. 2015;100(2):475–82.CrossRefPubMed
24.
go back to reference Neumann T, et al. Trabecular bone score in type 1 diabetes—a cross-sectional study. Osteoporos Int. 2016;27(1):127–33.CrossRefPubMed Neumann T, et al. Trabecular bone score in type 1 diabetes—a cross-sectional study. Osteoporos Int. 2016;27(1):127–33.CrossRefPubMed
26.
go back to reference Vashishth D. The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep. 2007;5(2):62–6.CrossRefPubMed Vashishth D. The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep. 2007;5(2):62–6.CrossRefPubMed
27.
go back to reference Monnier VM, Kohn RR, Cerami A. Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad Sci. 1984;81(2):583–7.CrossRefPubMed Monnier VM, Kohn RR, Cerami A. Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad Sci. 1984;81(2):583–7.CrossRefPubMed
28.
go back to reference Tang S, et al. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. 2009;20(6):887–94.CrossRefPubMed Tang S, et al. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. 2009;20(6):887–94.CrossRefPubMed
29.
go back to reference Burghardt AJ, 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.CrossRefPubMedPubMedCentral Burghardt AJ, 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.CrossRefPubMedPubMedCentral
30.
go back to reference Holzer G, et al. Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res. 2009;24(3):468–74.CrossRefPubMed Holzer G, et al. Hip fractures and the contribution of cortical versus trabecular bone to femoral neck strength. J Bone Miner Res. 2009;24(3):468–74.CrossRefPubMed
31.
go back to reference Pritchard JM, et al. Association of larger holes in the trabecular bone at the distal radius in postmenopausal women with type 2 diabetes mellitus compared to controls. Arthritis Care Res. 2012;64(1):83–91.CrossRef Pritchard JM, et al. Association of larger holes in the trabecular bone at the distal radius in postmenopausal women with type 2 diabetes mellitus compared to controls. Arthritis Care Res. 2012;64(1):83–91.CrossRef
32.
go back to reference Armas LA, et al. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2012;50(1):91–6.CrossRefPubMed Armas LA, et al. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2012;50(1):91–6.CrossRefPubMed
33.
go back to reference Niu T, Rosen CJ. The insulin-like growth factor-I gene and osteoporosis: a critical appraisal. Gene. 2005;361:38–56.CrossRefPubMed Niu T, Rosen CJ. The insulin-like growth factor-I gene and osteoporosis: a critical appraisal. Gene. 2005;361:38–56.CrossRefPubMed
34.
go back to reference Garnero P, Sornay-Rendu E, Delmas PD. Low serum IGF-1 and occurrence of osteoporotic fractures in postmenopausal women. Lancet. 2000;355(9207):898–9.CrossRefPubMed Garnero P, Sornay-Rendu E, Delmas PD. Low serum IGF-1 and occurrence of osteoporotic fractures in postmenopausal women. Lancet. 2000;355(9207):898–9.CrossRefPubMed
36.
go back to reference Nielson CM, et al. BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2011;26(3):496–502.CrossRefPubMed Nielson CM, et al. BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2011;26(3):496–502.CrossRefPubMed
37.
go back to reference Johansson H, et al. A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res. 2014;29(1):223–33.CrossRefPubMed Johansson H, et al. A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res. 2014;29(1):223–33.CrossRefPubMed
38.
go back to reference Sornay-Rendu E, et al. In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des femmes de Lyon (OFELY) study. J Bone Miner Res. 2013;28(7):1679–87.CrossRefPubMed Sornay-Rendu E, et al. In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des femmes de Lyon (OFELY) study. J Bone Miner Res. 2013;28(7):1679–87.CrossRefPubMed
39.
go back to reference Bredella MA, et al. Determinants of bone mineral density in obese premenopausal women. Bone. 2011;48(4):748–54.CrossRefPubMed Bredella MA, et al. Determinants of bone mineral density in obese premenopausal women. Bone. 2011;48(4):748–54.CrossRefPubMed
40.
go back to reference Cohen A, et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab. 2013;98(6):2562–72.CrossRefPubMedPubMedCentral Cohen A, et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab. 2013;98(6):2562–72.CrossRefPubMedPubMedCentral
Metadata
Title
Effect of diabetes on BMD and TBS values as determinants of bone health in the elderly: Bushehr Elderly Health program
Authors
Mahbube Ebrahimpur
Farshad Sharifi
Farzaneh Amini Nezhad
Mohammad Bagherzadeh
Afshin Ostovar
Gita Shafiee
Ramin Heshmat
Neda Mehrdad
Faride Razi
Patricia Khashayar
Iraj Nabipour
Bagher Larijani
Publication date
01-06-2019
Publisher
Springer International Publishing
Published in
Journal of Diabetes & Metabolic Disorders / Issue 1/2019
Electronic ISSN: 2251-6581
DOI
https://doi.org/10.1007/s40200-019-00395-1

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