Osteoporosis International

, Volume 29, Issue 3, pp 733–739 | Cite as

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

  • V. N. ShahEmail author
  • R. Sippl
  • P. Joshee
  • L. Pyle
  • W. M. Kohrt
  • I. E. Schauer
  • J. K. Snell-Bergeon
Original Article



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.


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.


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.


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.


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.


Bone mineral density Fracture Insulin resistance and abdominal obesity Osteoporosis Trabecular bone score Type 1 diabetes 



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.

Compliance with ethical standards

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.

Supplementary material

198_2017_4353_MOESM1_ESM.docx (12 kb)
Supplementary Table 1 (DOCX 12 kb).


  1. 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. CrossRefPubMedGoogle Scholar
  2. 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. CrossRefPubMedGoogle Scholar
  3. 3.
    Dhaon P, Shah VN (2014) Type 1 diabetes and osteoporosis: A review of literature. Indian J Endocrinol Metab 18(2):159–165. CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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. CrossRefPubMedGoogle Scholar
  6. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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. CrossRefPubMedGoogle Scholar
  8. 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. CrossRefPubMedGoogle Scholar
  9. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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. CrossRefPubMedGoogle Scholar
  11. 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. CrossRefPubMedGoogle Scholar
  12. 12.
    Schacter GI, Leslie WD (2017) DXA-Based Measurements in Diabetes: Can They Predict Fracture Risk? Calcif Tissue Int 100(2):150–164. CrossRefPubMedGoogle Scholar
  13. 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. CrossRefPubMedGoogle Scholar
  14. 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. CrossRefPubMedGoogle Scholar
  15. 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. CrossRefPubMedGoogle Scholar
  16. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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. CrossRefPubMedGoogle Scholar
  20. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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. CrossRefPubMedGoogle Scholar
  22. 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. CrossRefPubMedGoogle Scholar
  23. 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. CrossRefPubMedGoogle Scholar
  24. 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. CrossRefPubMedGoogle Scholar
  25. 25.
    Reid IR (2002) Relationships among body mass, its components, and bone. Bone 31(5):547–555. CrossRefPubMedGoogle Scholar
  26. 26.
    Gonnelli S, Caffarelli C, Nuti R (2014) Obesity and fracture risk. Clin Cases Miner Bone Metab 11(1):9–14. PubMedPubMedCentralGoogle Scholar
  27. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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. CrossRefPubMedGoogle Scholar
  29. 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. CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2017

Authors and Affiliations

  • V. N. Shah
    • 1
    Email author
  • R. Sippl
    • 1
  • P. Joshee
    • 1
  • L. Pyle
    • 1
    • 2
  • W. M. Kohrt
    • 3
    • 4
    • 5
    • 6
  • I. E. Schauer
    • 4
    • 5
    • 6
  • J. K. Snell-Bergeon
    • 1
  1. 1.Barbara Davis Center for DiabetesUniversity of Colorado Anschutz Medical CampusAuroraUSA
  2. 2.Department of Biostatistics and Informatics, Colorado School of Public HealthUniversity of Colorado Anschutz Medical CampusAuroraUSA
  3. 3.Division of Geriatric Medicine, Department of MedicineUniversity of Colorado Anschutz Medical CampusAuroraUSA
  4. 4.Division of Endocrinology, Metabolism and Diabetes, Department of Medicine, Anschutz Medical CampusUniversity of ColoradoAuroraUSA
  5. 5.Endocrinology Section, Department of Medicine, Denver VA Medical CenterDenverUSA
  6. 6.Eastern Colorado Geriatrics Research, Education, and Clinical CenterDenverUSA

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