Skip to main content
Top
Published in:

09-05-2024 | Type 2 Diabetes | Original Article

Prediction model for low bone mass mineral density in type 2 diabetes: an observational cross-sectional study

Authors: Cheng Ji, Jie Ma, Lingjun Sun, Xu Sun, Lijuan Liu, Lijun Wang, Weihong Ge, Yan Bi

Published in: Endocrine | Issue 1/2024

Login to get access

Abstract

Purpose

Considering the prevalence of type 2 diabetes (T2D), osteoporosis should be considered a serious complication. However, an effective tool for the assessment of low bone mass mineral density (BMD) in T2D patients is not currently available. Therefore, the aim of our study was to establish a simple-to-use risk assessment tool by exploring risk factors for low BMD in T2D patients.

Methods

This study included 436 patients with a low BMD and 381 patients with a normal BMD. Multiple logistic regression analysis was performed to evaluate risk factors for low BMD in T2D patients. A nomogram was then developed from these results. A receiver operating characteristic (ROC) curve, calibration plot, and goodness-of-fit test were used to validate the nomogram. The clinical utility of the nomogram was also assessed.

Results

Multivariate logistic regression indicated that age, sex, education, body mass index (BMI), fasting C-peptide, high-density cholesterol (HDL), alkaline phosphatase (ALP), estimated glomerular filtration rate (eGFR), and type I collagen carboxy terminal peptide (S-CTX) were independent predictors for low BMD in T2D patients. The nomogram was developed from these variables using both the unadjusted area under the curve (AUC) and the bootstrap-corrected AUC (0.828). Calibration plots and the goodness-of-fit test demonstrated that the nomogram was well calibrated.

Conclusions

The nomogram-illustrated model can be used by clinicians to easily predict the risk of low BMD in T2D patients. Our study also revealed that common factors are independent predictors of low BMD risk. Our results provide a new strategy for the prediction, investigation, and facilitation of low BMD in T2D patients.
Literature
1.
go back to reference P. Saeedi, I. Petersohn, P. Salpea, B. Malanda, S. Karuranga, N. Unwin et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res. Clin. Pract. 157, 107843 (2019)CrossRefPubMed P. Saeedi, I. Petersohn, P. Salpea, B. Malanda, S. Karuranga, N. Unwin et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res. Clin. Pract. 157, 107843 (2019)CrossRefPubMed
2.
go back to reference V. Tai, W. Leung, A. Grey, I.R. Reid, M.J. Bolland, Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ 351, h4183 (2015)CrossRefPubMedPubMedCentral V. Tai, W. Leung, A. Grey, I.R. Reid, M.J. Bolland, Calcium intake and bone mineral density: systematic review and meta-analysis. BMJ 351, h4183 (2015)CrossRefPubMedPubMedCentral
3.
go back to reference I. Perez-Diaz, G. Sebastian-Barajas, Z.G. Hernandez-Flores, R. Rivera-Moscoso, H.K. Osorio-Landa, A. Flores-Rebollar, The impact of vitamin D levels on glycemic control and bone mineral density in postmenopausal women with type 2 diabetes. J. Endocrinol. Investig. 38, 1365–1372 (2015)CrossRef I. Perez-Diaz, G. Sebastian-Barajas, Z.G. Hernandez-Flores, R. Rivera-Moscoso, H.K. Osorio-Landa, A. Flores-Rebollar, The impact of vitamin D levels on glycemic control and bone mineral density in postmenopausal women with type 2 diabetes. J. Endocrinol. Investig. 38, 1365–1372 (2015)CrossRef
4.
go back to reference P. Jackuliak, J. Payer, Osteoporosis, fractures, and diabetes. Int. J. Endocrinol. 2014, 1–10 (2014).CrossRef P. Jackuliak, J. Payer, Osteoporosis, fractures, and diabetes. Int. J. Endocrinol. 2014, 1–10 (2014).CrossRef
5.
go back to reference A. H. Mohammed, Sweet Bones: The pathogenesis of bone alteration in diabetes. J. Diabetes Res. 2016, 1–5 (2016). A. H. Mohammed, Sweet Bones: The pathogenesis of bone alteration in diabetes. J. Diabetes Res. 2016, 1–5 (2016).
6.
go back to reference N. Bonnet, Bone-derived factors: a new gateway to regulate glycemia. Calcif. Tissue Int. 100, 174–183 (2017)CrossRefPubMed N. Bonnet, Bone-derived factors: a new gateway to regulate glycemia. Calcif. Tissue Int. 100, 174–183 (2017)CrossRefPubMed
7.
go back to reference Z. VoVokó, K. Gáspár, A. Inotai, C. Horváth, K. Bors, G. Speer, Osteoporotic fractures may impair life as much as the complications of diabetes. J. Eval. Clin. Pract. 23, 1375–1380 (2017)CrossRef Z. VoVokó, K. Gáspár, A. Inotai, C. Horváth, K. Bors, G. Speer, Osteoporotic fractures may impair life as much as the complications of diabetes. J. Eval. Clin. Pract. 23, 1375–1380 (2017)CrossRef
8.
go back to reference J. Panula, H. Pihlajamäki, V.M. Mattila, P. Jaatinen, T. Vahlberg, P. Aarnio et al. Mortality and cause of death in hip fracture patients aged 65 or older: a population-based study. BMC Musculoskelet. Disord. 12, 105 (2011)CrossRefPubMedPubMedCentral J. Panula, H. Pihlajamäki, V.M. Mattila, P. Jaatinen, T. Vahlberg, P. Aarnio et al. Mortality and cause of death in hip fracture patients aged 65 or older: a population-based study. BMC Musculoskelet. Disord. 12, 105 (2011)CrossRefPubMedPubMedCentral
9.
go back to reference R. Hasserius, M.K. Karlsson, B. Jonsson, I. Redlund-Johnell, O. Johnell, Long-term morbidity and mortality after a clinically diagnosed vertebral fracture in the elderly–a 12-and 22-year follow-up of 257 patients. Calcif. Tissue Int. 76, 235–242 (2005)CrossRefPubMed R. Hasserius, M.K. Karlsson, B. Jonsson, I. Redlund-Johnell, O. Johnell, Long-term morbidity and mortality after a clinically diagnosed vertebral fracture in the elderly–a 12-and 22-year follow-up of 257 patients. Calcif. Tissue Int. 76, 235–242 (2005)CrossRefPubMed
10.
go back to reference E. Hernlund, A. Svedbom, M. Ivergård, J. Compston, C. Cooper, J. Stenmark et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch. Osteoporos. 8, 136 (2013)CrossRefPubMedPubMedCentral E. Hernlund, A. Svedbom, M. Ivergård, J. Compston, C. Cooper, J. Stenmark et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch. Osteoporos. 8, 136 (2013)CrossRefPubMedPubMedCentral
11.
go back to reference L. Si, T.M. Winzenberg, Q. Jiang, M. Chen, A.J. Palmer, Projection of osteoporosis-related fractures and costs in China: 2010-2050. Osteoporos. Int. 26, 1929–1937 (2015)CrossRefPubMed L. Si, T.M. Winzenberg, Q. Jiang, M. Chen, A.J. Palmer, Projection of osteoporosis-related fractures and costs in China: 2010-2050. Osteoporos. Int. 26, 1929–1937 (2015)CrossRefPubMed
12.
go back to reference J. Starup-Linde, M. Frost, P. Vestergaard, B. Abrahamsen, Epidemiology of fractures in diabetes. Calcif. Tissue Int. 100, 109–121 (2017)CrossRefPubMed J. Starup-Linde, M. Frost, P. Vestergaard, B. Abrahamsen, Epidemiology of fractures in diabetes. Calcif. Tissue Int. 100, 109–121 (2017)CrossRefPubMed
13.
go back to reference R. Tibshirani, Regression shrinkage and selection via the lasso: a retrospective. J. R. Stat. Soc.: Ser. B (Stat. Methodol.) 73, 273–282 (2011)CrossRef R. Tibshirani, Regression shrinkage and selection via the lasso: a retrospective. J. R. Stat. Soc.: Ser. B (Stat. Methodol.) 73, 273–282 (2011)CrossRef
14.
go back to reference S.H. Tella, J.C. Gallagher, Prevention and treatment of postmenopausal osteoporosis. J. Steroid Biochem. Mol. Biol. 142, 155–170 (2014)CrossRefPubMed S.H. Tella, J.C. Gallagher, Prevention and treatment of postmenopausal osteoporosis. J. Steroid Biochem. Mol. Biol. 142, 155–170 (2014)CrossRefPubMed
15.
go back to reference P. Garnero, E. Sornay-Rendu, F. Duboeuf, P.D. Delmas, Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. J. Bone Miner. Res. 14, 1614–1621 (2011)CrossRef P. Garnero, E. Sornay-Rendu, F. Duboeuf, P.D. Delmas, Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. J. Bone Miner. Res. 14, 1614–1621 (2011)CrossRef
16.
go back to reference C. De-Laet, J.A. Kanis, A. Odén, H. Johanson, O. Johnell, P. Delmas et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos. Int. 16, 1330–1338 (2005)CrossRefPubMed C. De-Laet, J.A. Kanis, A. Odén, H. Johanson, O. Johnell, P. Delmas et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos. Int. 16, 1330–1338 (2005)CrossRefPubMed
17.
go back to reference V. Benetou, P. Orfanos, D. Feskanich, K. Michaëlsson, U. Pettersson-Kymmer, L.A. Ahmed et al. Education, marital status, and risk of hip fractures in older men and women: the CHANCES project. Osteoporos. Int. 26, 1733–1746 (2015)CrossRefPubMed V. Benetou, P. Orfanos, D. Feskanich, K. Michaëlsson, U. Pettersson-Kymmer, L.A. Ahmed et al. Education, marital status, and risk of hip fractures in older men and women: the CHANCES project. Osteoporos. Int. 26, 1733–1746 (2015)CrossRefPubMed
18.
go back to reference H. Nakagawa, M. Kamimura, K. Takahara, H. Hashidate, A. Kawaguchi, S. Uchiyama et al. Changes in total alkaline phosphatase level after hip fracture: comparison between femoral neck and trochanter fractures. J. Orthop. Sci. 11, 135–139 (2006)CrossRefPubMed H. Nakagawa, M. Kamimura, K. Takahara, H. Hashidate, A. Kawaguchi, S. Uchiyama et al. Changes in total alkaline phosphatase level after hip fracture: comparison between femoral neck and trochanter fractures. J. Orthop. Sci. 11, 135–139 (2006)CrossRefPubMed
19.
go back to reference K.Y. Kang, Y.S. Hong, S.H. Park, J.H. Ju, Increased serum alkaline phosphatase levels correlate with high disease activity and low bone mass mineral density in patients with axial spondyloarthritis. Semin. Arthritis Rheum. 45, 202–207 (2015)CrossRefPubMed K.Y. Kang, Y.S. Hong, S.H. Park, J.H. Ju, Increased serum alkaline phosphatase levels correlate with high disease activity and low bone mass mineral density in patients with axial spondyloarthritis. Semin. Arthritis Rheum. 45, 202–207 (2015)CrossRefPubMed
20.
go back to reference M.A. Hansen, K. Overgaard, B.J. Riis, C. Christiansen, Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study. BMJ 303, 961–964 (1991)CrossRefPubMedPubMedCentral M.A. Hansen, K. Overgaard, B.J. Riis, C. Christiansen, Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study. BMJ 303, 961–964 (1991)CrossRefPubMedPubMedCentral
21.
go back to reference M. Li, Y. Li, W. Deng, Z. Zhang, Z. Deng, Y. Hu et al. Chinese bone turnover marker study: reference ranges for C-terminal telopeptide of type I collagen and procollagen I N-terminal peptide by age and gender. PLoS One 9, e103841 (2014)CrossRefPubMedPubMedCentral M. Li, Y. Li, W. Deng, Z. Zhang, Z. Deng, Y. Hu et al. Chinese bone turnover marker study: reference ranges for C-terminal telopeptide of type I collagen and procollagen I N-terminal peptide by age and gender. PLoS One 9, e103841 (2014)CrossRefPubMedPubMedCentral
22.
go back to reference K.C. Tsolis, E.S. Bei, I. Papathanasiou, F. Kostopoulou, V. Gkretsi, K. kalantzaki et al. Comparative proteomic analysis of hypertrophic chondrocytes in osteoarthritis. Clin. Proteom. 12, 12 (2015)CrossRef K.C. Tsolis, E.S. Bei, I. Papathanasiou, F. Kostopoulou, V. Gkretsi, K. kalantzaki et al. Comparative proteomic analysis of hypertrophic chondrocytes in osteoarthritis. Clin. Proteom. 12, 12 (2015)CrossRef
23.
24.
go back to reference N.I. Papachristou, H.C. Blair, K.E. Kypreos, D.J. Papachristou, High-density lipoprotein (HDL) metabolism and bone mass. J. Endocrinol. 233, R95–R107 (2017)CrossRefPubMedPubMedCentral N.I. Papachristou, H.C. Blair, K.E. Kypreos, D.J. Papachristou, High-density lipoprotein (HDL) metabolism and bone mass. J. Endocrinol. 233, R95–R107 (2017)CrossRefPubMedPubMedCentral
25.
go back to reference I.K. Jeong, S.W. Cho, S.W. Kim, H.J. Choi, K.S. Park, S.Y. Kim et al. Lipid profiles and bone mineral density in pre- and postmenopausal women in Korea. Calcif. Tissue Int. 87, 507–512 (2010)CrossRefPubMed I.K. Jeong, S.W. Cho, S.W. Kim, H.J. Choi, K.S. Park, S.Y. Kim et al. Lipid profiles and bone mineral density in pre- and postmenopausal women in Korea. Calcif. Tissue Int. 87, 507–512 (2010)CrossRefPubMed
26.
go back to reference K.C. Kim, D.H. Shin, S.Y. Lee, J.A. Im, D.C. Lee, Relation between obesity and bone mineral density and vertebral fractures in Korean postmenopausal women. Yonsei Med. J. 51, 857–863 (2010)CrossRefPubMedPubMedCentral K.C. Kim, D.H. Shin, S.Y. Lee, J.A. Im, D.C. Lee, Relation between obesity and bone mineral density and vertebral fractures in Korean postmenopausal women. Yonsei Med. J. 51, 857–863 (2010)CrossRefPubMedPubMedCentral
27.
go back to reference S. Nagpal, S. Na, R. Rathnachalam, Noncalcemic actions of vitamin D receptor ligands. Endocr. Rev. 26, 662–687 (2005)CrossRefPubMed S. Nagpal, S. Na, R. Rathnachalam, Noncalcemic actions of vitamin D receptor ligands. Endocr. Rev. 26, 662–687 (2005)CrossRefPubMed
28.
go back to reference A.G. Pittas, J. Lau, F.B. Hu, B. Dawson-Hughes, The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 92, 2017–2029 (2007)CrossRefPubMed A.G. Pittas, J. Lau, F.B. Hu, B. Dawson-Hughes, The role of vitamin D and calcium in type 2 diabetes. A systematic review and meta-analysis. J. Clin. Endocrinol. Metab. 92, 2017–2029 (2007)CrossRefPubMed
29.
go back to reference Y. Song, L. Wang, A.G. Pittas, L.C. Del Gobbo, C. Zhang, J.E. Manson et al. Blood 25-Hydroxy Vitamin D Levels and Incident Type 2 Diabetes. Diabetes Care 36, 1422–1428 (2013)CrossRefPubMedPubMedCentral Y. Song, L. Wang, A.G. Pittas, L.C. Del Gobbo, C. Zhang, J.E. Manson et al. Blood 25-Hydroxy Vitamin D Levels and Incident Type 2 Diabetes. Diabetes Care 36, 1422–1428 (2013)CrossRefPubMedPubMedCentral
30.
go back to reference R. BaBasu, E. Breda, A.L. Oberg, C.C. Powell, C. Dalla Man, A. Basu et al. Mechanisms of the age-associated deterioration in glucose tolerance: contribution of alterations in insulin secretion, action, and clearance. Diabetes 52, 1738–1748 (2003)CrossRef R. BaBasu, E. Breda, A.L. Oberg, C.C. Powell, C. Dalla Man, A. Basu et al. Mechanisms of the age-associated deterioration in glucose tolerance: contribution of alterations in insulin secretion, action, and clearance. Diabetes 52, 1738–1748 (2003)CrossRef
31.
go back to reference A. Udristioiu, Alkaline Phosphatase Isoenzymes and Leukocyte Alkaline Phosphatase Score in Patients with Acute and Chronic Disease: a Brief Review. Br. J. Med. Med. Res. 4, 340–350 (2013)CrossRef A. Udristioiu, Alkaline Phosphatase Isoenzymes and Leukocyte Alkaline Phosphatase Score in Patients with Acute and Chronic Disease: a Brief Review. Br. J. Med. Med. Res. 4, 340–350 (2013)CrossRef
32.
go back to reference S. Baim, P.D. Miller, Perspective: assessing the clinical utility of serum CTX in postmenopausal osteoporosis and its use in predicting risk of osteonecrosis of the jaw. J. Bone Min. Res 24, 561–574 (2009)CrossRef S. Baim, P.D. Miller, Perspective: assessing the clinical utility of serum CTX in postmenopausal osteoporosis and its use in predicting risk of osteonecrosis of the jaw. J. Bone Min. Res 24, 561–574 (2009)CrossRef
33.
go back to reference S. Vasikaran, C. Cooper, R. Eastell, A. Griesmacher, H.A. Morris, T. Trenti et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin. Chem. Lab Med. 49, 1271–1274 (2011)CrossRefPubMed S. Vasikaran, C. Cooper, R. Eastell, A. Griesmacher, H.A. Morris, T. Trenti et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin. Chem. Lab Med. 49, 1271–1274 (2011)CrossRefPubMed
34.
go back to reference P. Garnero, E. Hausherr, M.C. Chapuy, C. Marcelli, H. Grandjean, C. Muller et al. Markers of bone resorption predict hip fracture in elderly women: the EPIDOS Prospective Study. J. Bone Min. Res. 11, 1531–1538 (1996)CrossRef P. Garnero, E. Hausherr, M.C. Chapuy, C. Marcelli, H. Grandjean, C. Muller et al. Markers of bone resorption predict hip fracture in elderly women: the EPIDOS Prospective Study. J. Bone Min. Res. 11, 1531–1538 (1996)CrossRef
35.
go back to reference N. Napoli, R. Strollo, D. Sprini, E. Maddaloni, G.B. Rini, E. Carmina, Serum 25-OH Vitamin D in relation to Bone Mineral Density and Bone Turnover. Int. J. Endocrinol. 2014, 487463 (2014)CrossRefPubMedPubMedCentral N. Napoli, R. Strollo, D. Sprini, E. Maddaloni, G.B. Rini, E. Carmina, Serum 25-OH Vitamin D in relation to Bone Mineral Density and Bone Turnover. Int. J. Endocrinol. 2014, 487463 (2014)CrossRefPubMedPubMedCentral
Metadata
Title
Prediction model for low bone mass mineral density in type 2 diabetes: an observational cross-sectional study
Authors
Cheng Ji
Jie Ma
Lingjun Sun
Xu Sun
Lijuan Liu
Lijun Wang
Weihong Ge
Yan Bi
Publication date
09-05-2024
Publisher
Springer US
Published in
Endocrine / Issue 1/2024
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-023-03500-w

Keynote series | Spotlight on menopause

Menopause can have a significant impact on the body, with effects ranging beyond the endocrine and reproductive systems. Learn about the systemic effects of menopause, so you can help patients in your clinics through the transition.   

Prof. Martha Hickey
Dr. Claudia Barth
Dr. Samar El Khoudary
Developed by: Springer Medicine
Watch now

Keynote webinar | Spotlight on adolescent vaping

Growing numbers of young people are using e-cigarettes, despite warnings of respiratory effects and addiction. How can doctors tackle the epidemic, and what health effects should you prepare to manage in your clinics?

Prof. Ann McNeill
Dr. Debbie Robson
Benji Horwell
Developed by: Springer Medicine
Watch now

Keynote webinar | Spotlight on modern management of frailty

Frailty has a significant impact on health and wellbeing, especially in older adults. Our experts explain the factors that contribute to the development of frailty and how you can manage the condition and reduce the risk of disability, dependency, and mortality in your patients.

Prof. Alfonso Cruz-Jentoft
Prof. Barbara C. van Munster
Prof. Mirko Petrovic
Developed by: Springer Medicine
Watch now

A quick guide to ECGs

Improve your ECG interpretation skills with this comprehensive, rapid, interactive course. Expert advice provides detailed feedback as you work through 50 ECGs covering the most common cardiac presentations to ensure your practice stays up to date. 

PD Dr. Carsten W. Israel
Developed by: Springer Medizin
Start the cases

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine
Read more