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Published in: Endocrine 2/2022

14-06-2022 | Insulins | Original Article

The relationship between estimated glucose disposal rate and bone turnover markers in type 2 diabetes mellitus

Authors: Zelin Li, Cuijuan Qi, Xiaoyu Pan, Yujiao Jia, Xuetong Zhao, Chenqian Deng, Shuchun Chen

Published in: Endocrine | Issue 2/2022

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Abstract

Purpose

To investigate the relationship between estimated glucose disposal rate (eGDR) and bone turnover markers in patients with type 2 diabetes mellitus (T2DM).

Materials and methods

This is a cross-sectional study, which recruited 549 patients with T2DM. The eGDRs of patients were calculated based on the presence of hypertension, glycated hemoglobin, and body mass index. All patients were divided into high-eGDR group and low-eGDR group using the median of eGDR as the boundary. The patients were further divided into two subgroups: males and postmenopausal females.

Results

The lower the eGDR, the more severe was insulin resistance. The levels of osteocalcin (OC), type I collagen carboxyl-terminal peptide (β-CTX), and type I procollagen amino-terminal peptide (PINP) were significantly lower in the low-eGDR group than those in the high-eGDR group. The eGDR was positively correlated with OC, β-CTX, and PINP in all patients, and in the male subgroups. In the postmenopausal female subgroup, there was no correlation between eGDR and OC, β-CTX, or PINP. In addition, this positive correlation remained after adjusting for other factors in multilinear regression analysis.

Conclusion

Our study was the first to demonstrate that eGDR is positively correlated with bone turnover markers in patients with T2DM. This correlation was observed among the male patients with T2DM but not among postmenopausal female patients with T2DM.
Literature
1.
go back to reference F. Alaei-Shahmiri, M.E. Khamseh, K. Manhoei, H. Yadegari, H. Kazemi et al. The optimal vitamin D cut-off value associated with hyperglycemia in an Iranian population. J. Diabetes Metab. Disord. 19, 5–12 (2020)PubMedCrossRef F. Alaei-Shahmiri, M.E. Khamseh, K. Manhoei, H. Yadegari, H. Kazemi et al. The optimal vitamin D cut-off value associated with hyperglycemia in an Iranian population. J. Diabetes Metab. Disord. 19, 5–12 (2020)PubMedCrossRef
2.
go back to reference H. Chang-Quan, D. Bi-Rong, H. Ping, L. Zhen-Chan, Insufficient renal 1-alpha hydroxylase and bone homeostasis in aged rats with insulin resistance or type 2 diabetes mellitus. J. Bone Miner. Metab. 26, 561–568 (2008)PubMedCrossRef H. Chang-Quan, D. Bi-Rong, H. Ping, L. Zhen-Chan, Insufficient renal 1-alpha hydroxylase and bone homeostasis in aged rats with insulin resistance or type 2 diabetes mellitus. J. Bone Miner. Metab. 26, 561–568 (2008)PubMedCrossRef
3.
go back to reference R. Nishtala, N. Kietsiriroje, Estimated glucose disposal rate demographics and clinical characteristics of young adults with type 1 diabetes mellitus: a cross-sectional pilot study. Diab. Vasc. Dis. Res. 17, 1479164120952321 (2020) R. Nishtala, N. Kietsiriroje, Estimated glucose disposal rate demographics and clinical characteristics of young adults with type 1 diabetes mellitus: a cross-sectional pilot study. Diab. Vasc. Dis. Res. 17, 1479164120952321 (2020)
4.
go back to reference K.V. Williams, J.R. Erbey, D. Becker, S. Arslanian, T.J. Orchard, Can clinical factors estimate insulin resistance in type 1 diabetes? Diabetes 49, 626–632 (2000)PubMedCrossRef K.V. Williams, J.R. Erbey, D. Becker, S. Arslanian, T.J. Orchard, Can clinical factors estimate insulin resistance in type 1 diabetes? Diabetes 49, 626–632 (2000)PubMedCrossRef
5.
go back to reference L.L. O’Mahoney, N. Kietsiriroje, Estimated glucose disposal rate as a candidate biomarker for thrombotic biomarkers in T1D: a pooled analysis. J. Endocrinol. Invest. 44, 2417–2426 (2021) L.L. O’Mahoney, N. Kietsiriroje, Estimated glucose disposal rate as a candidate biomarker for thrombotic biomarkers in T1D: a pooled analysis. J. Endocrinol. Invest. 44, 2417–2426 (2021)
6.
go back to reference J.J. Chillarón, A. Goday, J.A. Flores-Le-Roux, D. Benaiges, M.J. Carrera et al. Estimated glucose disposal rate in assessment of the metabolic syndrome and microvascular complications in patients with type 1 diabetes. J. Clin. Endocrinol. Metab. 94, 3530–3534 (2009)PubMedCrossRef J.J. Chillarón, A. Goday, J.A. Flores-Le-Roux, D. Benaiges, M.J. Carrera et al. Estimated glucose disposal rate in assessment of the metabolic syndrome and microvascular complications in patients with type 1 diabetes. J. Clin. Endocrinol. Metab. 94, 3530–3534 (2009)PubMedCrossRef
7.
go back to reference A. Zabala, V. Darsalia, M. Lind, A.M. Svensson, S. Franzén et al. Estimated glucose disposal rate and risk of stroke and mortality in type 2 diabetes: a nationwide cohort study. Cardiovascular Diabetol. 20, 202 (2021)CrossRef A. Zabala, V. Darsalia, M. Lind, A.M. Svensson, S. Franzén et al. Estimated glucose disposal rate and risk of stroke and mortality in type 2 diabetes: a nationwide cohort study. Cardiovascular Diabetol. 20, 202 (2021)CrossRef
8.
go back to reference T. Nyström, M.J. Holzmann, B. Eliasson, A.M. Svensson, J. Kuhl et al. Estimated glucose disposal rate and long-term survival in type 2 diabetes after coronary artery bypass grafting. Heart Vessels 32, 269–278 (2017) T. Nyström, M.J. Holzmann, B. Eliasson, A.M. Svensson, J. Kuhl et al. Estimated glucose disposal rate and long-term survival in type 2 diabetes after coronary artery bypass grafting. Heart Vessels 32, 269–278 (2017)
9.
go back to reference P. Vestergaard, Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos. Int. 18, 427–444 (2007)PubMedCrossRef P. Vestergaard, Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes–a meta-analysis. Osteoporos. Int. 18, 427–444 (2007)PubMedCrossRef
10.
go back to reference K. Hygum, J. Starup-Linde, T. Harsløf, P. Vestergaard, B.L. Langdahl, MECHANISMS IN ENDOCRINOLOGY: diabetes mellitus, a state of low bone turnover – a systematic review and meta-analysis. Eur. J. Endocrinol. 176, R137–r157 (2017)PubMedCrossRef K. Hygum, J. Starup-Linde, T. Harsløf, P. Vestergaard, B.L. Langdahl, MECHANISMS IN ENDOCRINOLOGY: diabetes mellitus, a state of low bone turnover – a systematic review and meta-analysis. Eur. J. Endocrinol. 176, R137–r157 (2017)PubMedCrossRef
11.
go back to reference J.Y. Lee, N.K. Lee, Up-regulation of cyclinD1 and Bcl2A1 by insulin is involved in osteoclast proliferation. Life Sci. 114, 57–61 (2014)PubMedCrossRef J.Y. Lee, N.K. Lee, Up-regulation of cyclinD1 and Bcl2A1 by insulin is involved in osteoclast proliferation. Life Sci. 114, 57–61 (2014)PubMedCrossRef
12.
go back to reference K. Fulzele, R.C. Riddle, D.J. DiGirolamo, X. Cao, C. Wan et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142, 309–319 (2010)PubMedPubMedCentralCrossRef K. Fulzele, R.C. Riddle, D.J. DiGirolamo, X. Cao, C. Wan et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142, 309–319 (2010)PubMedPubMedCentralCrossRef
13.
go back to reference K.T. Tonks, C.P. White, J.R. Center, D. Samocha-Bonet, J.R. Greenfield, Bone turnover is suppressed in insulin resistance, independent of adiposity. J. Clin. Endocrinol. Metab. 102, 1112–1121 (2017)PubMedCrossRef K.T. Tonks, C.P. White, J.R. Center, D. Samocha-Bonet, J.R. Greenfield, Bone turnover is suppressed in insulin resistance, independent of adiposity. J. Clin. Endocrinol. Metab. 102, 1112–1121 (2017)PubMedCrossRef
15.
go back to reference V.V. Shanbhogue, J.S. Finkelstein, M.L. Bouxsein, E.W. Yu, Association between insulin resistance and bone structure in nondiabetic postmenopausal women. J. Clin. Endocrinol. Metab. 101, 3114–3122 (2016)PubMedPubMedCentralCrossRef V.V. Shanbhogue, J.S. Finkelstein, M.L. Bouxsein, E.W. Yu, Association between insulin resistance and bone structure in nondiabetic postmenopausal women. J. Clin. Endocrinol. Metab. 101, 3114–3122 (2016)PubMedPubMedCentralCrossRef
16.
go back to reference E.M. Dennison, H.E. Syddall, A. Aihie Sayer, S. Craighead, D.I. Phillips et al. 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 (2004)PubMedCrossRef E.M. Dennison, H.E. Syddall, A. Aihie Sayer, S. Craighead, D.I. Phillips et al. 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 (2004)PubMedCrossRef
17.
go back to reference S. Huang, M. Kaw, M.T. Harris, N. Ebraheim, M.F. McInerney et al. Decreased osteoclastogenesis and high bone mass in mice with impaired insulin clearance due to liver-specific inactivation to CEACAM1. Bone 46, 1138–1145 (2010)PubMedPubMedCentralCrossRef S. Huang, M. Kaw, M.T. Harris, N. Ebraheim, M.F. McInerney et al. Decreased osteoclastogenesis and high bone mass in mice with impaired insulin clearance due to liver-specific inactivation to CEACAM1. Bone 46, 1138–1145 (2010)PubMedPubMedCentralCrossRef
18.
go back to reference S.K. Kunutsor, T.A. Apekey, J.A. Laukkanen, Association of serum total osteocalcin with type 2 diabetes and intermediate metabolic phenotypes: systematic review and meta-analysis of observational evidence. Eur. J. Epidemiol. 30, 599–614 (2015)PubMedCrossRef S.K. Kunutsor, T.A. Apekey, J.A. Laukkanen, Association of serum total osteocalcin with type 2 diabetes and intermediate metabolic phenotypes: systematic review and meta-analysis of observational evidence. Eur. J. Epidemiol. 30, 599–614 (2015)PubMedCrossRef
19.
go back to reference S. Yano, T. Nabika, A. Nagai, T. Hamano, M. Yamasaki et al. Interrelationship between glucose metabolism and undercarboxylated osteocalcin: a cross-sectional study in a community-dwelling population. Asia Pac. J. Clin. Nutr. 24, 489–495 (2015)PubMed S. Yano, T. Nabika, A. Nagai, T. Hamano, M. Yamasaki et al. Interrelationship between glucose metabolism and undercarboxylated osteocalcin: a cross-sectional study in a community-dwelling population. Asia Pac. J. Clin. Nutr. 24, 489–495 (2015)PubMed
20.
go back to reference S.W. Lee, H.H. Jo, M.R. Kim, J.H. Kim, Y.O. You, Association between osteocalcin and metabolic syndrome in postmenopausal women. Arch. Gynecol. Obstet. 292, 673–681 (2015)PubMedCrossRef S.W. Lee, H.H. Jo, M.R. Kim, J.H. Kim, Y.O. You, Association between osteocalcin and metabolic syndrome in postmenopausal women. Arch. Gynecol. Obstet. 292, 673–681 (2015)PubMedCrossRef
21.
go back to reference W.W. Hu, Y.H. Ke, J.W. He, W.Z. Fu, Y.J. Liu et al. Serum osteocalcin levels are inversely associated with plasma glucose and body mass index in healthy Chinese women. Acta Pharmacol. Sin. 35, 1521–1526 (2014)PubMedPubMedCentralCrossRef W.W. Hu, Y.H. Ke, J.W. He, W.Z. Fu, Y.J. Liu et al. Serum osteocalcin levels are inversely associated with plasma glucose and body mass index in healthy Chinese women. Acta Pharmacol. Sin. 35, 1521–1526 (2014)PubMedPubMedCentralCrossRef
22.
go back to reference G.S. Kim, Y. Jekal, H.S. Kim, J.A. Im, J.Y. Park et al. Reduced serum total osteocalcin is associated with central obesity in Korean children. Obes. Res. Clin. Pract. 8, e201–e298 (2014)PubMedCrossRef G.S. Kim, Y. Jekal, H.S. Kim, J.A. Im, J.Y. Park et al. Reduced serum total osteocalcin is associated with central obesity in Korean children. Obes. Res. Clin. Pract. 8, e201–e298 (2014)PubMedCrossRef
23.
go back to reference K. Mori, M. Emoto, K. Motoyama, E. Lee, S. Yamada et al. Undercarboxylated osteocalcin does not correlate with insulin resistance as assessed by euglycemic hyperinsulinemic clamp technique in patients with type 2 diabetes mellitus. Diabetol. Metab. Syndr. 4, 53 (2012)PubMedPubMedCentralCrossRef K. Mori, M. Emoto, K. Motoyama, E. Lee, S. Yamada et al. Undercarboxylated osteocalcin does not correlate with insulin resistance as assessed by euglycemic hyperinsulinemic clamp technique in patients with type 2 diabetes mellitus. Diabetol. Metab. Syndr. 4, 53 (2012)PubMedPubMedCentralCrossRef
24.
go back to reference X.Y. Ma, F.Q. Chen, H. Hong, X.J. Lv, M. Dong et al. The relationship between serum osteocalcin concentration and glucose and lipid metabolism in patients with type 2 diabetes mellitus – the role of osteocalcin in energy metabolism. Ann. Nutr. Metab. 66, 110–116 (2015)PubMedCrossRef X.Y. Ma, F.Q. Chen, H. Hong, X.J. Lv, M. Dong et al. The relationship between serum osteocalcin concentration and glucose and lipid metabolism in patients with type 2 diabetes mellitus – the role of osteocalcin in energy metabolism. Ann. Nutr. Metab. 66, 110–116 (2015)PubMedCrossRef
25.
go back to reference K.M. Bador, L.D. Wee, S.A. Halim, M.F. Fadi, P. Santhiran et al. Serum osteocalcin in subjects with metabolic syndrome and central obesity. Diabetes Metab. Syndr. 10, S42–S45 (2016)PubMedCrossRef K.M. Bador, L.D. Wee, S.A. Halim, M.F. Fadi, P. Santhiran et al. Serum osteocalcin in subjects with metabolic syndrome and central obesity. Diabetes Metab. Syndr. 10, S42–S45 (2016)PubMedCrossRef
26.
go back to reference Q. Wang, B. Zhang, Y. Xu, H. Xu, N. Zhang, The relationship between serum osteocalcin concentration and glucose metabolism in patients with type 2 diabetes mellitus. Int. J. Endocrinol. 2013, 842598 (2013)PubMedPubMedCentral Q. Wang, B. Zhang, Y. Xu, H. Xu, N. Zhang, The relationship between serum osteocalcin concentration and glucose metabolism in patients with type 2 diabetes mellitus. Int. J. Endocrinol. 2013, 842598 (2013)PubMedPubMedCentral
27.
go back to reference H. Guo, C. Wang, B. Jiang, S. Ge, J. Cai et al. Association of insulin resistance and β-cell function with bone turnover biomarkers in dysglycemia patients. Front. Endocrinol. 12, 554604 (2021)CrossRef H. Guo, C. Wang, B. Jiang, S. Ge, J. Cai et al. Association of insulin resistance and β-cell function with bone turnover biomarkers in dysglycemia patients. Front. Endocrinol. 12, 554604 (2021)CrossRef
28.
go back to reference Z. Feldbrin, M. Shargorodsky, Bone remodelling markers in hypertensive patients with and without diabetes mellitus: link between bone and glucose metabolism. Diabetes Metab. Res. Rev. 31, 752–757 (2015)PubMedCrossRef Z. Feldbrin, M. Shargorodsky, Bone remodelling markers in hypertensive patients with and without diabetes mellitus: link between bone and glucose metabolism. Diabetes Metab. Res. Rev. 31, 752–757 (2015)PubMedCrossRef
29.
go back to reference G.M. Reaven, Pathophysiology of insulin resistance in human disease. Physiological Rev. 75, 473–486 (1995)CrossRef G.M. Reaven, Pathophysiology of insulin resistance in human disease. Physiological Rev. 75, 473–486 (1995)CrossRef
30.
go back to reference A. Fraser, R. Harris, N. Sattar, S. Ebrahim, G. Davey Smith et al. Alanine aminotransferase, gamma-glutamyltransferase, and incident diabetes: the British Women’s Heart and Health Study and meta-analysis. Diabetes Care 32, 741–750 (2009)PubMedPubMedCentralCrossRef A. Fraser, R. Harris, N. Sattar, S. Ebrahim, G. Davey Smith et al. Alanine aminotransferase, gamma-glutamyltransferase, and incident diabetes: the British Women’s Heart and Health Study and meta-analysis. Diabetes Care 32, 741–750 (2009)PubMedPubMedCentralCrossRef
31.
go back to reference A.J. Hanley, L.E. Wagenknecht, A. Festa, R.B. D’Agostino Jr., S.M. Haffner, Alanine aminotransferase and directly measured insulin sensitivity in a multiethnic cohort: the Insulin Resistance Atherosclerosis Study. Diabetes Care 30, 1819–1827 (2007)PubMedCrossRef A.J. Hanley, L.E. Wagenknecht, A. Festa, R.B. D’Agostino Jr., S.M. Haffner, Alanine aminotransferase and directly measured insulin sensitivity in a multiethnic cohort: the Insulin Resistance Atherosclerosis Study. Diabetes Care 30, 1819–1827 (2007)PubMedCrossRef
32.
go back to reference L. Aguirre, N. Napoli, D. Waters, C. Qualls, D.T. Villareal et al. Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J. Clin. Endocrinol. Metab. 99, 3290–3297 (2014)PubMedPubMedCentralCrossRef L. Aguirre, N. Napoli, D. Waters, C. Qualls, D.T. Villareal et al. Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J. Clin. Endocrinol. Metab. 99, 3290–3297 (2014)PubMedPubMedCentralCrossRef
33.
go back to reference F.L. Bilotta, B. Arcidiacono, S. Messineo, M. Greco, E. Chiefari et al. Insulin and osteocalcin: further evidence for a mutual cross-talk. Endocrine 59, 622–632 (2018) F.L. Bilotta, B. Arcidiacono, S. Messineo, M. Greco, E. Chiefari et al. Insulin and osteocalcin: further evidence for a mutual cross-talk. Endocrine 59, 622–632 (2018)
34.
go back to reference L. Wang, T. Li, J. Liu, X. Wu, H. Wang et al. Association between glycosylated hemoglobin A1c and bone biochemical markers in type 2 diabetic postmenopausal women: a cross-sectional study. BMC Endocr. Disord. 19, 31 (2019) L. Wang, T. Li, J. Liu, X. Wu, H. Wang et al. Association between glycosylated hemoglobin A1c and bone biochemical markers in type 2 diabetic postmenopausal women: a cross-sectional study. BMC Endocr. Disord. 19, 31 (2019)
35.
go back to reference W. Wang, X. Zhang, J. Zheng, J. Yang, High glucose stimulates adipogenic and inhibits osteogenic differentiation in MG-63 cells through cAMP/protein kinase A/extracellular signal-regulated kinase pathway. Mol. Cell. Biochem. 338, 115–122 (2010)PubMedCrossRef W. Wang, X. Zhang, J. Zheng, J. Yang, High glucose stimulates adipogenic and inhibits osteogenic differentiation in MG-63 cells through cAMP/protein kinase A/extracellular signal-regulated kinase pathway. Mol. Cell. Biochem. 338, 115–122 (2010)PubMedCrossRef
36.
go back to reference P. Lakatos, B. Szili, B. Bakos, I. Takacs, Z. Putz et al. Thyroid hormones, glucocorticoids, insulin, and bone. Handb. Exp. Pharmacol. 262, 93–120 (2020)PubMedCrossRef P. Lakatos, B. Szili, B. Bakos, I. Takacs, Z. Putz et al. Thyroid hormones, glucocorticoids, insulin, and bone. Handb. Exp. Pharmacol. 262, 93–120 (2020)PubMedCrossRef
37.
go back to reference M. Alikhani, Z. Alikhani, C. Boyd, C.M. MacLellan, M. Raptis et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40, 345–353 (2007)PubMedCrossRef M. Alikhani, Z. Alikhani, C. Boyd, C.M. MacLellan, M. Raptis et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40, 345–353 (2007)PubMedCrossRef
38.
go back to reference L.F. Liu, W.J. Shen, Z.H. Zhang, L.J. Wang, F.B. Kraemer, Adipocytes decrease Runx2 expression in osteoblastic cells: roles of PPARγ and adiponectin. J. Cell. Physiol. 225, 837–845 (2010)PubMedCrossRef L.F. Liu, W.J. Shen, Z.H. Zhang, L.J. Wang, F.B. Kraemer, Adipocytes decrease Runx2 expression in osteoblastic cells: roles of PPARγ and adiponectin. J. Cell. Physiol. 225, 837–845 (2010)PubMedCrossRef
39.
go back to reference P. Vestergaard, Diabetes and osteoporosis – cause for concern? Front. Endocrinol. 5, 53 (2014)CrossRef P. Vestergaard, Diabetes and osteoporosis – cause for concern? Front. Endocrinol. 5, 53 (2014)CrossRef
40.
go back to reference C. Ma, K.T. Tonks, J.R. Center, D. Samocha-Bonet, J.R. Greenfield, Complex interplay among adiposity, insulin resistance and bone health. Clin. Obes. 8, 131–139 (2018)PubMedCrossRef C. Ma, K.T. Tonks, J.R. Center, D. Samocha-Bonet, J.R. Greenfield, Complex interplay among adiposity, insulin resistance and bone health. Clin. Obes. 8, 131–139 (2018)PubMedCrossRef
41.
go back to reference S. Rathinavelu, C. Guidry-Elizondo, J. Banu, Molecular modulation of osteoblasts and osteoclasts in type 2. Diabetes 2018, 6354787 (2018) S. Rathinavelu, C. Guidry-Elizondo, J. Banu, Molecular modulation of osteoblasts and osteoclasts in type 2. Diabetes 2018, 6354787 (2018)
42.
go back to reference K. Baek, H.R. Hwang, H.J. Park, A. Kwon, A.S. Qadir et al. TNF-α upregulates sclerostin expression in obese mice fed a high-fat diet. J. Cell. Physiol. 229, 640–650 (2014)PubMedCrossRef K. Baek, H.R. Hwang, H.J. Park, A. Kwon, A.S. Qadir et al. TNF-α upregulates sclerostin expression in obese mice fed a high-fat diet. J. Cell. Physiol. 229, 640–650 (2014)PubMedCrossRef
43.
go back to reference V. Boschert, M. van Dinther, S. Weidauer, K. van Pee, E.M. Muth et al. Mutational analysis of sclerostin shows importance of the flexible loop and the cystine-knot for Wnt-signaling inhibition. PloS One 8, e81710 (2013)PubMedPubMedCentralCrossRef V. Boschert, M. van Dinther, S. Weidauer, K. van Pee, E.M. Muth et al. Mutational analysis of sclerostin shows importance of the flexible loop and the cystine-knot for Wnt-signaling inhibition. PloS One 8, e81710 (2013)PubMedPubMedCentralCrossRef
44.
go back to reference Z. Yao, L. Xing, C. Qin, E.M. Schwarz, B.F. Boyce, Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J. Biol. Chem. 283, 9917–9924 (2008)PubMedPubMedCentralCrossRef Z. Yao, L. Xing, C. Qin, E.M. Schwarz, B.F. Boyce, Osteoclast precursor interaction with bone matrix induces osteoclast formation directly by an interleukin-1-mediated autocrine mechanism. J. Biol. Chem. 283, 9917–9924 (2008)PubMedPubMedCentralCrossRef
45.
go back to reference C. Conte, S. Epstein, N. Napoli, Insulin resistance and bone: a biological partnership. Acta Diabetol. 55, 305–314 (2018) C. Conte, S. Epstein, N. Napoli, Insulin resistance and bone: a biological partnership. Acta Diabetol. 55, 305–314 (2018)
46.
go back to reference Y. Bao, X. Ma, R. Yang, F. Wang, Y. Hao et al. Inverse relationship between serum osteocalcin levels and visceral fat area in Chinese men. J. Clin. Endocrinol. Metab. 98, 345–351 (2013)PubMedCrossRef Y. Bao, X. Ma, R. Yang, F. Wang, Y. Hao et al. Inverse relationship between serum osteocalcin levels and visceral fat area in Chinese men. J. Clin. Endocrinol. Metab. 98, 345–351 (2013)PubMedCrossRef
47.
go back to reference S. Muruganandan, C.J. Sinal, The impact of bone marrow adipocytes on osteoblast and osteoclast differentiation. IUBMB Life 66, 147–155 (2014)PubMedCrossRef S. Muruganandan, C.J. Sinal, The impact of bone marrow adipocytes on osteoblast and osteoclast differentiation. IUBMB Life 66, 147–155 (2014)PubMedCrossRef
48.
go back to reference X.G. Han, D.W. Wang, Z.G. Bi, F. Gao, Regulatory effect of estrogen receptor-α-mediated Wnt/β-catenin signaling pathway on osteoblast proliferation. J. Biol. Regul. Homeost. Agents 30, 381–387 (2016)PubMed X.G. Han, D.W. Wang, Z.G. Bi, F. Gao, Regulatory effect of estrogen receptor-α-mediated Wnt/β-catenin signaling pathway on osteoblast proliferation. J. Biol. Regul. Homeost. Agents 30, 381–387 (2016)PubMed
49.
go back to reference J.A. Im, B.P. Yu, J.Y. Jeon, S.H. Kim, Relationship between osteocalcin and glucose metabolism in postmenopausal women. Clin. Chim. Acta 396, 66–69 (2008)PubMedCrossRef J.A. Im, B.P. Yu, J.Y. Jeon, S.H. Kim, Relationship between osteocalcin and glucose metabolism in postmenopausal women. Clin. Chim. Acta 396, 66–69 (2008)PubMedCrossRef
50.
go back to reference Y.C. Hwang, I.K. Jeong, K.J. Ahn, H.Y. Chung, Circulating osteocalcin level is associated with improved glucose tolerance, insulin secretion and sensitivity independent of the plasma adiponectin level. Osteoporos. Int. 23, 1337–1342 (2012)PubMedCrossRef Y.C. Hwang, I.K. Jeong, K.J. Ahn, H.Y. Chung, Circulating osteocalcin level is associated with improved glucose tolerance, insulin secretion and sensitivity independent of the plasma adiponectin level. Osteoporos. Int. 23, 1337–1342 (2012)PubMedCrossRef
51.
go back to reference P.D. Sarkar, A.B. Choudhury, Relationships between serum osteocalcin levels versus blood glucose, insulin resistance and markers of systemic inflammation in central Indian type 2 diabetic patients. Eur. Rev. Med. Pharmacol. Sci. 17, 1631–1635 (2013)PubMed P.D. Sarkar, A.B. Choudhury, Relationships between serum osteocalcin levels versus blood glucose, insulin resistance and markers of systemic inflammation in central Indian type 2 diabetic patients. Eur. Rev. Med. Pharmacol. Sci. 17, 1631–1635 (2013)PubMed
52.
go back to reference M. Zhou, X. Ma, H. Li, X. Pan, J. Tang et al. Serum osteocalcin concentrations in relation to glucose and lipid metabolism in Chinese individuals. Eur. J. Endocrinol. 161, 723–729 (2009)PubMedCrossRef M. Zhou, X. Ma, H. Li, X. Pan, J. Tang et al. Serum osteocalcin concentrations in relation to glucose and lipid metabolism in Chinese individuals. Eur. J. Endocrinol. 161, 723–729 (2009)PubMedCrossRef
Metadata
Title
The relationship between estimated glucose disposal rate and bone turnover markers in type 2 diabetes mellitus
Authors
Zelin Li
Cuijuan Qi
Xiaoyu Pan
Yujiao Jia
Xuetong Zhao
Chenqian Deng
Shuchun Chen
Publication date
14-06-2022
Publisher
Springer US
Published in
Endocrine / Issue 2/2022
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-022-03090-z

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