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Review Article
Bone Metabolism
Skeletal Fragility in Type 2 Diabetes Mellitus
Jakob Starup-Linde, Katrine Hygum, Bente Lomholt Langdahl
Endocrinol Metab. 2018;33(3):339-351.   Published online September 18, 2018
DOI: https://doi.org/10.3803/EnM.2018.33.3.339
  • 5,757 View
  • 101 Download
  • 26 Web of Science
  • 23 Crossref
AbstractAbstract PDFPubReader   ePub   

Type 2 diabetes (T2D) is associated with an increased risk of fracture, which has been reported in several epidemiological studies. However, bone mineral density in T2D is increased and underestimates the fracture risk. Common risk factors for fracture do not fully explain the increased fracture risk observed in patients with T2D. We propose that the pathogenesis of increased fracture risk in T2D is due to low bone turnover caused by osteocyte dysfunction resulting in bone microcracks and fractures. Increased levels of sclerostin may mediate the low bone turnover and may be a novel marker of increased fracture risk, although further research is needed. An impaired incretin response in T2D may also affect bone turnover. Accumulation of advanced glycosylation endproducts may also impair bone strength. Concerning antidiabetic medication, the glitazones are detrimental to bone health and associated with increased fracture risk, and the sulphonylureas may increase fracture risk by causing hypoglycemia. So far, the results on the effect of other antidiabetics are ambiguous. No specific guideline for the management of bone disease in T2D is available and current evidence on the effects of antiosteoporotic medication in T2D is sparse. The aim of this review is to collate current evidence of the pathogenesis, detection and treatment of diabetic bone disease.

Citations

Citations to this article as recorded by  
  • Effects of Exogenous GIP and GLP-2 on Bone Turnover in Individuals With Type 2 Diabetes
    Kirsa Skov-Jeppesen, Charlotte B Christiansen, Laura S Hansen, Johanne A Windeløv, Nora Hedbäck, Lærke S Gasbjerg, Morten Hindsø, Maria S Svane, Sten Madsbad, Jens J Holst, Mette M Rosenkilde, Bolette Hartmann
    The Journal of Clinical Endocrinology & Metabolism.2024;[Epub]     CrossRef
  • The association between type 2 diabetes mellitus/prediabetes status and femoral neck bone mineral density in old adults
    Bo Wang, Chenhao Shi, Zhongxin Zhu
    Journal of Orthopaedic Surgery.2024;[Epub]     CrossRef
  • Bone parameters in T1D and T2D assessed by DXA and HR-pQCT – A cross-sectional study: The DIAFALL study
    Nicklas Højgaard-hessellund Rasmussen, Jakob Dal, Annika Vestergaard Kvist, Joop P. van den Bergh, Morten Hasselstrøm Jensen, Peter Vestergaard
    Bone.2023; 172: 116753.     CrossRef
  • Clinical risk factors analysis and prevention of osteoporosis as a complication of diabetes
    Jiaojiao Wang, Hang Li, Haihong Zhu, Xinyan Xie, Qiyue Zheng, Jian Qu, Haiyan Yuan, Ting Liu, Qiong Lu
    International Journal of Diabetes in Developing Countries.2023;[Epub]     CrossRef
  • Effects of a Lifestyle Intervention on Bone Turnover in Persons with Type 2 Diabetes: A Post Hoc Analysis of the U-TURN Trial
    JULIE ABILDGAARD, METTE YUN JOHANSEN, KIRSA SKOV-JEPPESEN, LARS BO ANDERSEN, KRISTIAN KARSTOFT, KATRINE BAGGE HANSEN, BOLETTE HARTMANN, JENS JUUL HOLST, BENTE KLARLUND PEDERSEN, MATHIAS RIED-LARSEN
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  • The Effects of 12-Weeks Whey Protein Supplements on Markers of Bone Turnover in Adults With Abdominal Obesity – A Post Hoc Analysis
    Rasmus Fuglsang-Nielsen, Elin Rakvaag, Peter Vestergaard, Kjeld Hermansen, Søren Gregersen, Jakob Starup-Linde
    Frontiers in Endocrinology.2022;[Epub]     CrossRef
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    Nicklas H. Rasmussen, Peter Vestergaard
    Best Practice & Research Clinical Rheumatology.2022; 36(3): 101779.     CrossRef
  • Do proximal hip geometry, trabecular microarchitecture, and prevalent vertebral fractures differ in postmenopausal women with type 2 diabetes mellitus? A cross-sectional study from a teaching hospital in southern India
    J. Paul, V. Devarapalli, J. T. Johnson, K. E. Cherian, F. K. Jebasingh, H. S. Asha, N. Kapoor, N. Thomas, T. V. Paul
    Osteoporosis International.2021; 32(8): 1585.     CrossRef
  • Investigation of Mechanical, Material, and Compositional Determinants of Human Trabecular Bone Quality in Type 2 Diabetes
    Praveer Sihota, Ram Naresh Yadav, Ruban Dhaliwal, Jagadeesh Chandra Bose, Vandana Dhiman, Deepak Neradi, Shailesh Karn, Sidhartha Sharma, Sameer Aggarwal, Vijay G Goni, Vishwajeet Mehandia, Deepak Vashishth, Sanjay Kumar Bhadada, Navin Kumar
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    Osteoporosis International.2021; 32(8): 1465.     CrossRef
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    Sabina Chaudhary Hauge, Bo Abrahamsen, Gunnar Gislason, Jonas Bjerring Olesen, Kristine Hommel, Ditte Hansen
    Bone.2021; 153: 116158.     CrossRef
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    Jeonghoon Ha, Yejee Lim, Mee Kyoung Kim, Hyuk-Sang Kwon, Ki-Ho Song, Seung Hyun Ko, Moo Il Kang, Sung Dae Moon, Ki-Hyun Baek
    Endocrinology and Metabolism.2021; 36(4): 895.     CrossRef
  • Can fingernail quality predict bone damage in Type 2 diabetes mellitus? a pilot study
    Praveer Sihota, Rimesh Pal, Ram Naresh Yadav, Deepak Neradi, Shailesh Karn, Vijay G. Goni, Siddhartha Sharma, Vishwajeet Mehandia, Sanjay Kumar Bhadada, Navin Kumar, Sudhaker D. Rao, Subburaman Mohan
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  • Do patients with diabetes have an increased risk of impaired fracture healing? A systematic review and meta‐analysis
    Zi‐chuan Ding, Wei‐nan Zeng, Xiao Rong, Zhi‐min Liang, Zong‐ke Zhou
    ANZ Journal of Surgery.2020; 90(7-8): 1259.     CrossRef
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    Orit Ofir, Assaf Buch, Vanessa Rouach, Rebecca Goldsmith, Naftali Stern, Efrat Monsonego-Ornan
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    N.H. Rasmussen, J. Dal, F. de Vries, J.P. van den Bergh, M.H. Jensen, P. Vestergaard
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  • Association of glycaemic variables with trabecular bone score in post‐menopausal women with type 2 diabetes mellitus
    B. Depczynski, P. Y. Liew, C. White
    Diabetic Medicine.2020; 37(9): 1545.     CrossRef
  • Understanding Bone Disease in Patients with Diabetic Kidney Disease: a Narrative Review
    Sabina Chaudhary Hauge, Morten Frost, Ditte Hansen
    Current Osteoporosis Reports.2020; 18(6): 727.     CrossRef
  • Falls and Fractures in Diabetes—More than Bone Fragility
    Nicklas Højgaard Rasmussen, Jakob Dal
    Current Osteoporosis Reports.2019; 17(3): 147.     CrossRef
  • Role of Metformin on Osteoblast Differentiation in Type 2 Diabetes
    Lin Jiating, Ji Buyun, Zhang Yinchang
    BioMed Research International.2019; 2019: 1.     CrossRef
  • An update on therapies for the treatment of diabetes-induced osteoporosis
    Sahar Mohsin, May MYH Baniyas, Reem SMH AlDarmaki, Kornélia Tekes, Huba Kalász, Ernest A. Adeghate
    Expert Opinion on Biological Therapy.2019; 19(9): 937.     CrossRef
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Original Article
Clinical Study
The Association of Higher Plasma Macrophage Migration Inhibitory Factor Levels with Lower Bone Mineral Density and Higher Bone Turnover Rate in Postmenopausal Women
Hyeonmok Kim, Seong Hee Ahn, Chaeho Shin, Seung Hun Lee, Beom-Jun Kim, Jung-Min Koh
Endocrinol Metab. 2016;31(3):454-461.   Published online July 26, 2016
DOI: https://doi.org/10.3803/EnM.2016.31.3.454
  • 3,833 View
  • 43 Download
  • 8 Web of Science
  • 9 Crossref
AbstractAbstract PDFSupplementary MaterialPubReader   
Background

Despite evidence from animal and clinical studies showing the detrimental effects of macrophage migration inhibitory factor (MIF) on bone metabolism, there are no clinical studies relating circulating MIF levels to osteoporosis-related phenotypes. This cross-sectional study investigated the association of plasma MIF with bone mineral density (BMD), bone turnover markers (BTMs), and prevalence of osteoporosis in postmenopausal Korean women.

Methods

A total of 246 women not taking any medications or diagnosed with any diseases that could affect bone metabolism were enrolled. BMD values at the lumbar spine, femoral neck, and total femur, and blood levels of MIF and BTMs were measured in all subjects. Osteoporosis was defined by World Health Organization criteria.

Results

Before and after adjustment for confounding variables, higher MIF levels were significantly associated with lower BMD values at all measured sites and higher levels of all BTMs. All BMD values and BTMs significantly changed in a dose-dependent fashion across increasing MIF quartile. When participants were divided into two groups according to osteoporosis status, postmenopausal women with osteoporosis demonstrated 24.2% higher plasma MIF levels than those without osteoporosis (P=0.041). The odds ratio per each standard deviation increment of MIF levels for prevalent osteoporosis was 1.32 (95% confidence interval, 1.01 to 1.73).

Conclusion

This study provides the first epidemiological evidence that higher plasma MIF may be associated with higher risk of osteoporosis resulting from lower bone mass and higher bone turnover rate, and thus it could be a potential biomarker of poor bone health outcomes in postmenopausal women.

Citations

Citations to this article as recorded by  
  • The role of MIF in periodontitis: A potential pathogenic driver, biomarker, and therapeutic target
    Tongfeng Fang, Liu Liu, Dongzhe Song, Dingming Huang
    Oral Diseases.2023;[Epub]     CrossRef
  • Variation of Bone Turnover Markers in Childhood and Adolescence
    Yiduo Zhang, Jing Zhang, Xiaocui Huang, Xingnan Yu, Ye Li, Fan Yu, Wenjie Zhou, Ziqing Li
    International Journal of Clinical Practice.2023; 2023: 1.     CrossRef
  • Modulation of Dopamine Receptors on Osteoblasts as a Possible Therapeutic Strategy for Inducing Bone Formation in Arthritis
    Elena Schwendich, Laura Salinas Tejedor, Gernot Schmitz, Markus Rickert, Jürgen Steinmeyer, Stefan Rehart, Styliani Tsiami, Jürgen Braun, Xenofon Baraliakos, Jörg Reinders, Elena Neumann, Ulf Müller-Ladner, Silvia Capellino
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    Elisabeth Gjefsen, Kristina Gervin, Guro Goll, Lars Christian Haugli Bråten, Monica Wigemyr, Hans Christian D Aass, Maria Dehli Vigeland, Elina Schistad, Linda Margareth Pedersen, Are Hugo Pripp, Kjersti Storheim, Kaja Kristine Selmer, John Anker Zwart
    RMD Open.2021; 7(2): e001726.     CrossRef
  • Potential Biomarkers to Improve the Prediction of Osteoporotic Fractures
    Beom-Jun Kim, Seung Hun Lee, Jung-Min Koh
    Endocrinology and Metabolism.2020; 35(1): 55.     CrossRef
  • Elevated Expression of Macrophage Migration Inhibitory Factor Promotes Inflammatory Bone Resorption Induced in a Mouse Model of Periradicular Periodontitis
    Mohammed Howait, Abdullah Albassam, Chiaki Yamada, Hajime Sasaki, Laila Bahammam, Mariane Maffei Azuma, Luciano Tavares Angelo Cintra, Abhay R. Satoskar, Satoru Yamada, Robert White, Toshihisa Kawai, Alexandru Movila
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    Seong-Eun Byun, Soonchul Lee, Ji Wan Kim, Yong-Chan Ha, Chul-Ho Kim, Cheungsoo Ha, Keun Jung Ryu, Jung-Min Koh, Hyung Kyung Kim, Jae Suk Chang
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    Won-Young Lee
    Endocrinology and Metabolism.2017; 32(1): 62.     CrossRef
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    Sun Wook Cho
    Endocrinology and Metabolism.2016; 31(3): 400.     CrossRef
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