Skip to main content

Advertisement

Log in

Trabecular bone quality is lower in adults with type 1 diabetes and is negatively associated with insulin resistance

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

We evaluated trabecular bone score (TBS) and factors affecting TBS in adults with type 1 diabetes (T1D) compared to age-, sex-, and body mass index (BMI)-matched adults without diabetes. Adults with T1D had lower TBS compared to controls. Abdominal obesity and insulin resistance are associated with lower TBS.

Introduction

We evaluated TBS, a non-invasive method to evaluate trabecular bone quality at the lumbar spine, in adults with T1D compared to age-, sex-, and BMI-matched adults without diabetes.

Methods

We calculated TBS from adults with T1D (n = 47) and controls (n = 47) who had a lumbar spine dual x-ray absorptiometry (DXA) at their third visit (2006–2009) of the ongoing “Coronary Artery Calcification in Type 1 Diabetes (CACTI) Study.” The linear relationships of TBS and bone mineral density (BMD) with hemoglobin A1c, blood pressure, lipids, and insulin resistance were evaluated using Pearson’s correlation coefficient. Multiple linear regression was used to test the association of TBS with sex and diabetes while adjusting for other potential confounders.

Results

TBS was significantly lower in adults with T1D compared to controls (1.42 ± 0.12 vs 1.44 ± 0.08, p = 0.02) after adjusting for age, sex, current smoking status, and lumbar spine BMD, despite no difference in lumbar spine BMD between the groups. Components of the metabolic syndrome, including diastolic blood pressure, BMI, triglycerides, and insulin resistance were negatively correlated with TBS among patients with T1D.

Conclusion

Trabecular bone score, an indirect measurement of trabecular bone quality, was lower in adults with T1D compared to controls. Components of metabolic syndrome and insulin resistance were associated with lower TBS in adults with T1D.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Pambianco G, Costacou T, Ellis D, Becker DJ, Klein R, Orchard TJ (2006) The 30-year natural history of type 1 diabetes complications: the Pittsburgh epidemiology of diabetes complications study experience. Diabetes 55(5):1463–1469. https://doi.org/10.2337/db05-1423

    Article  CAS  PubMed  Google Scholar 

  2. Harding JL, Shaw JE, Peeters A, Guiver T, Davidson S, Magliano DJ (2014) Mortality trends among people with type 1 and type 2 diabetes in Australia: 1997-2010. Diabetes Care 37(9):2579–2586. https://doi.org/10.2337/dc14-0096

    Article  PubMed  Google Scholar 

  3. Dhaon P, Shah VN (2014) Type 1 diabetes and osteoporosis: A review of literature. Indian J Endocrinol Metab 18(2):159–165. https://doi.org/10.4103/2230-8210.129105

    Article  PubMed  PubMed Central  Google Scholar 

  4. Shah VN, Shah CS, Snell-Bergeon JK (2015) Risk for fracture in type 1 diabetes: a meta-analysis and review of the literature. Diabet Med 32(9):1134–1142. https://doi.org/10.1111/dme.12734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP, Lindsay RS, McKnight J, Pearson D, Philip S, Wild SH, Colhoun HM (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29(5):1054–1060. https://doi.org/10.1002/jbmr.2118

    Article  PubMed  Google Scholar 

  6. Weber DR, Haynes K, Leonard MB, Willi SM, Denburg MR (2015) Type 1 diabetes is associated with an increased risk of fracture across the life span: a population-based cohort study using The Health Improvement Network (THIN). Diabetes Care 38(10):1913–1920. https://doi.org/10.2337/dc15-0783

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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(4):427–444. https://doi.org/10.1007/s00198-006-0253-4

    Article  CAS  PubMed  Google Scholar 

  8. Shah VN, Harrall KK, Shah CS, Gallo TL, Joshee P, Snell-Bergeon JK, Kohrt WM (2017) Bone mineral density at femoral neck and lumbar spine in adults with type 1 diabetes: a meta-analysis and review of the literature. Osteoporos Int 28(Jun 3):2601–2610. https://doi.org/10.1007/s00198-017-4097-x

    Article  CAS  PubMed  Google Scholar 

  9. Harvey NC, Glüer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C, Kendler D, Lamy O, Laslop A, Camargos BM, Reginster JY, Rizzoli R, Kanis JA (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224. https://doi.org/10.1016/j.bone.2015.05.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Riggs BL, Melton LJ, Robb RA, Camp JJ, Atkinson EJ, McDaniel L, Amin S, Rouleau PA, Khosla S (2008) A population-based assessment of rates of bone loss at multiple skeletal sites: evidence for substantial trabecular bone loss in young adult women and men. J Bone Miner Res 23(2):205–214. https://doi.org/10.1359/jbmr.071020

    Article  PubMed  Google Scholar 

  11. Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J Clin Densitom 18(3):309–330. https://doi.org/10.1016/j.jocd.2015.06.008

    Article  PubMed  Google Scholar 

  12. Schacter GI, Leslie WD (2017) DXA-Based Measurements in Diabetes: Can They Predict Fracture Risk? Calcif Tissue Int 100(2):150–164. https://doi.org/10.1007/s00223-016-0191-x

    Article  CAS  PubMed  Google Scholar 

  13. Choi YJ, Ock SY, Chung YS (2016) Trabecular Bone Score (TBS) and TBS-Adjusted Fracture Risk Assessment Tool are Potential Supplementary Tools for the Discrimination of Morphometric Vertebral Fractures in Postmenopausal Women With Type 2 Diabetes. J Clin Densitom 19(4):507–514. https://doi.org/10.1016/j.jocd.2016.04.001

    Article  PubMed  Google Scholar 

  14. Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25(7):1969–1973. https://doi.org/10.1007/s00198-014-2704-7

    Article  CAS  PubMed  Google Scholar 

  15. Neumann T, Lodes S, Kästner B, Lehmann T, Hans D, Lamy O, Müller UA, Wolf G, Sämann A (2016) Trabecular bone score in type 1 diabetes-a cross-sectional study. Osteoporos Int 27(1):127–133. https://doi.org/10.1007/s00198-015-3222-y

    Article  CAS  PubMed  Google Scholar 

  16. Kim K-C, Shin D-H, Lee S-Y, Im J-A, Lee D-C (2010) Relation between obesity and bone mineral density and vertebral fractures in Korean postmenopausal women. Yonsei Med J 51(6):857–863. https://doi.org/10.3349/ymj.2010.51.6.857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the rancho Bernardo study. Osteoporos Int 18(10):1337–1344. https://doi.org/10.1007/s00198-007-0385-1

    Article  Google Scholar 

  18. Srikanthan P, Crandall CJ, Miller-Martinez D, Seeman TE, Greendale GA, Binkley N, Karlamangla AS (2014) Insulin resistance and bone strength: findings from the study of midlife in the United States. J Bone Miner Res 29(4):796–803. https://doi.org/10.1002/jbmr.2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Cree-Green M, Newcomer BR, Brown MS, Baumgartner AD, Bergman B, Drew B, Regensteiner JG, Pyle L, Reusch JEB, Nadeau KJ (2015) Delayed skeletal muscle mitochondrial ADP recovery in youth with type 1 diabetes relates to muscle insulin resistance. Diabetes 64(2):383–392. https://doi.org/10.2337/db14-0765

    Article  CAS  PubMed  Google Scholar 

  20. Pereira RI, Snell-Bergeon JK, Erickson C, Schauer IE, Bergman BC, Rewers M, Maahs DM (2012) Adiponectin dysregulation and insulin resistance in type 1 diabetes. J Clin Endocrinol Metab 97(4):E642–E647. https://doi.org/10.1210/jc.2011-2542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Schauer IE, Snell-Bergeon JK, Bergman BC, Maahs DM, Kretowski A, Eckel RH, Rewers M (2011) Insulin resistance, defective insulin-mediated fatty acid suppression, and coronary artery calcification in subjects with and without type 1 diabetes: the CACTI study. Diabetes 60(1):306–314. https://doi.org/10.2337/db10-0328

    Article  CAS  PubMed  Google Scholar 

  22. Dabelea D, Kinney G, Snell-Bergeon JK, Hokanson JE, Eckel RH, Ehrlich J, Garg S, Hamman RF, Rewers M, Coronary Artery Calcification in Type 1 Diabetes Study (2003) Coronary Artery Calcification in Type 1 Diabetes Study. Effect of type 1 diabetes on the gender difference in coronary artery calcification: a role for insulin resistance? The coronary artery calcification in type 1 diabetes (CACTI) study. Diabetes 52(11):2833–2839. https://doi.org/10.2337/diabetes.52.11.2833

    Article  CAS  PubMed  Google Scholar 

  23. Snell-Bergeon JK, Hokanson JE, Jensen L, MacKenzie T, Kinney G, Dabelea D, Eckel RH, Ehrlich J, Garg S, Rewers M (2003) Progression of coronary artery calcification in type 1 diabetes: the importance of glycemic control. Diabetes Care 26(10):2923–2928. https://doi.org/10.2337/diacare.26.10.2923

    Article  PubMed  Google Scholar 

  24. Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S (2008) International Society for Clinical Densitometry 2007 Adult and Pediatric Official Positions. Bone 43(6):1115–1121. https://doi.org/10.1016/j.bone.2008.08.106

    Article  PubMed  Google Scholar 

  25. Reid IR (2002) Relationships among body mass, its components, and bone. Bone 31(5):547–555. https://doi.org/10.1016/S8756-3282(02)00864-5

    Article  CAS  PubMed  Google Scholar 

  26. Gonnelli S, Caffarelli C, Nuti R (2014) Obesity and fracture risk. Clin Cases Miner Bone Metab 11(1):9–14. https://doi.org/10.11138/ccmbm/2014.11.1.009

    PubMed  PubMed Central  Google Scholar 

  27. Liu Y-h, Xu Y, Wen Y-B, Guan K, Ling W-h, He L-p et al (2013) Association of Weight-Adjusted Body fat and fat Distribution with bone mineral density in middle-aged Chinese adults: a cross-sectional study. PLoS One 8(5):e63339. https://doi.org/10.1371/journal.pone.0063339

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Specht BJ, Wadwa RP, Snell-Bergeon JK, Nadeau KJ, Bishop FK, Maahs DM (2013) Estimated insulin sensitivity and cardiovascular disease risk factors in adolescents with and without type 1 diabetes. J Pediatr 162(2):297–301. https://doi.org/10.1016/j.jpeds.2012.07.036

    Article  CAS  PubMed  Google Scholar 

  29. Schmidt FM, Weschenfelder J, Sander C, Minkwitz J, Thormann J, Chittka T, Mergl R, Kirkby KC, Faßhauer M, Stumvoll M, Holdt LM, Teupser D, Hegerl U, Himmerich H (2015) Inflammatory cytokines in general and central obesity and modulating effects of physical activity. PLoS One 10(3):e0121971. https://doi.org/10.1371/journal.pone.0121971

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The study was supported from NHLBI grants HL61753, HL79611, and HL113029, DERC Clinical Investigation Core P30 DK57516, JDRF grant 17-2013-313, American Diabetes Association Career Development Award to Dr. Snell-Bergeon (7-13-CD-50) and a Center for Women’ Health Research Seed Grant to Dr. Shah. The study was performed at the Adult CTRC at UCD supported by NIH-M01-RR00051 and CTSA Grant UL1 TR001082 (IES), at the Barbara Davis Center for Childhood Diabetes and at Colorado Heart Imaging Center in Denver, CO.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. N. Shah.

Ethics declarations

All subjects provided informed consent and the study was approved by the Colorado Multiple Institutional Review Board.

Conflict of interest

VNS, RS, PJ, LP, PJ, WMK, IES, and JKS declare no conflict of interest related to this work. JKS is the guarantor of this work.

Electronic supplementary material

Supplementary Table 1

(DOCX 12 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shah, V.N., Sippl, R., Joshee, P. et al. Trabecular bone quality is lower in adults with type 1 diabetes and is negatively associated with insulin resistance. Osteoporos Int 29, 733–739 (2018). https://doi.org/10.1007/s00198-017-4353-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-017-4353-0

Keywords

Navigation