pp 1–7 | Cite as

Trabecular bone score: a useful clinical tool for the evaluation of skeletal health in women of short stature

  • Pedro Paulo Martins Alvarenga
  • Barbara Campolina SilvaEmail author
  • Mariana Picoli Diniz
  • Milena Bellei Leite
  • Caroline Alves Moreira da Silva
  • Jessica de Cássia Mendes Eleutério
  • Maria Marta Sarquis Soares
  • John P. Bilezikian
  • Bruno Muzzi Camargos
Original Article



Areal bone mineral density (aBMD) by DXA is underestimated in those with smaller bones and overestimated in those with larger bones. Trabecular bone score (TBS) predicts fracture risk, and is not influenced by bone size. The aim of this study was to evaluate TBS and BMD in women with short stature.


We retrospectively analyzed DXA scans of all women aged 50–90 years with short stature (<144 cm) obtained in a single center, from 2006 to 2016. The comparison group comprised women >161 cm in height, matched for age and LS BMD, selected from the same database.


The study population included 342 women. The two groups were similar in age, and aBMD at the LS and total hip. Femoral neck aBMD was lower in cases than in taller women. In contrast, TBS was higher in women with short stature than in their taller counterparts (1.347 ± 0.102 vs. 1.250 ± 0.110; p < 0.001). Bone mineral apparent density (BMAD) and the LS TBS-adjusted BMD T-score were also significantly higher in shorter than in taller women. From the entire cohort, 121 women (67 cases) were osteoporotic by aBMD determinations. Among these subjects, TBS was also greater in cases (1.303 ± 0.103) than in women with standard height (1.190 ± 0.099; p < 0.001). Despite being considered osteoporotic, 36% of short women, but none of the taller ones, had a normal TBS.


TBS can be a useful adjunct to aBMD for assessing bone quality in short women, in whom aBMD measurement tends to read lower, and, thus could overestimate fracture risk.


Trabecular bone score DXA Short stature Fracture risk Osteoporosis 


Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Statement

This work was partially supported by the Foundation for Research Support of the State of Minas Gerais—FAPEMIG (to PPMA and MMSS). This study consisted of review of medical records, and involved no more than minimal risks to subjects. The Institutional Review Board approved the protocol. All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.


  1. 1.
    P.M. Camacho, S.M. Petak, N. Binkley, B.L. Clarke, S.T. Harris, D.L. Hurley, M. Kleerekoper, E.M. Lewiecki, P.D. Miller, H.S. Narula, R. Pessah-Pollack, V. Tangpricha, S.J. Wimalawansa, N.B. Watts, American Association of Clinical Endocrinologists and American College of Endocrinology Clinical Practice Guidelines for the diagnosis and treatment of postmenopausal osteoporosis—2016. Endocr. Pract. 22(Suppl 4), 1–42 (2016). CrossRefGoogle Scholar
  2. 2.
    O. Johnell, J.A. Kanis, An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos. Int. 17(12), 1726–1733 (2006). CrossRefGoogle Scholar
  3. 3.
    M.L. Bouxsein, Bone quality: where do we go from here? Osteoporos. Int. 14(Suppl 5), S118–S127 (2003). CrossRefGoogle Scholar
  4. 4.
    D.R. Carter, M.L. Bouxsein, R. Marcus, New approaches for interpreting projected bone densitometry data. J. Bone Miner. Res. 7(2), 137–145 (1992). CrossRefGoogle Scholar
  5. 5.
    L.K. Bachrach, R. Marcus, S.M. Ott, A.L. Rosenbloom, O. Vasconez, V. Martinez, A.L. Martinez, R.G. Rosenfeld, J. Guevara-Aguirre, Bone mineral, histomorphometry, and body composition in adults with growth hormone receptor deficiency. J. Bone Miner. Res. 13(3), 415–421 (1998). CrossRefGoogle Scholar
  6. 6.
    M.E. Armstrong, O. Kirichek, B.J. Cairns, J. Green, G.K. Reeves; Valerie Beral for the Million Women Study, C., Relationship of height to site-specific fracture risk in postmenopausal women. J. Bone Miner. Res. 31(4), 725–731 (2016). CrossRefGoogle Scholar
  7. 7.
    D. Hans, N. Barthe, S. Boutroy, L. Pothuaud, R. Winzenrieth, M.A. Krieg, Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J. Clin. Densitom. 14(3), 302–312 (2011). CrossRefGoogle Scholar
  8. 8.
    B.C. Silva, W.D. Leslie, H. Resch, O. Lamy, O. Lesnyak, N. Binkley, E.V. McCloskey, J.A. Kanis, J.P. Bilezikian, Trabecular bone score: a noninvasive analytical method based upon the DXA image. J. Bone Miner. Res. 29(3), 518–530 (2014)CrossRefGoogle Scholar
  9. 9.
    S. Boutroy, D. Hans, E. Sornay-Rendu, N. Vilayphiou, R. Winzenrieth, R. Chapurlat, Trabecular bone score improves fracture risk prediction in non-osteoporotic women: the OFELY study. Osteoporos. Int. 24(1), 77–85 (2013). CrossRefGoogle Scholar
  10. 10.
    D. Hans, A.L. Goertzen, M.A. Krieg, W.D. Leslie, Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J. Bone Miner. Res. 26(11), 2762–2769 (2011). CrossRefGoogle Scholar
  11. 11.
    M. Iki, Y. Fujita, J. Tamaki, K. Kouda, A. Yura, Y. Sato, J.S. Moon, R. Winzenrieth, N. Okamoto, N. Kurumatani, Trabecular bone score may improve FRAX(R) prediction accuracy for major osteoporotic fractures in elderly Japanese men: the Fujiwara-kyo Osteoporosis Risk in Men (FORMEN) Cohort Study. Osteoporos. Int. 26(6), 1841–1848 (2015). CrossRefGoogle Scholar
  12. 12.
    M. Iki, J. Tamaki, E. Kadowaki, Y. Sato, N. Dongmei, R. Winzenrieth, S. Kagamimori, Y. Kagawa, H. Yoneshima, Trabecular bone score (TBS) predicts vertebral fractures in Japanese women over 10 years independently of bone density and prevalent vertebral deformity: the Japanese Population-Based Osteoporosis (JPOS) cohort study. J. Bone Miner. Res. 29(2), 399–407 (2014). CrossRefGoogle Scholar
  13. 13.
    W.D. Leslie, B. Aubry-Rozier, L.M. Lix, S.N. Morin, S.R. Majumdar, D. Hans, Spine bone texture assessed by trabecular bone score (TBS) predicts osteoporotic fractures in men: the Manitoba Bone Density Program. Bone 67, 10–14 (2014). CrossRefGoogle Scholar
  14. 14.
    J.T. Schousboe, T. Vo, B.C. Taylor, P.M. Cawthon, A.V. Schwartz, D.C. Bauer, E.S. Orwoll, N.E. Lane, E. Barrett-Connor, K.E. Ensrud; Osteoporotic Fractures in Men Mr, O.S.S.R.G., Prediction of incident major osteoporotic and hip fractures by trabecular bone score (TBS) and prevalent radiographic vertebral fracture in older men. J. Bone Miner. Res. 31(3), 690–697 (2016). CrossRefGoogle Scholar
  15. 15.
    E.V. McCloskey, A. Odén, N.C. Harvey, W.D. Leslie, D. Hans, H. Johansson, R. Barkmann, S. Boutroy, J. Brown, R. Chapurlat, A meta‐analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J. Bone Miner. Res. 31(5), 940–948 (2016)CrossRefGoogle Scholar
  16. 16.
    M. Garcia-Hoyos, M.T. Garcia-Unzueta, D. de Luis, C. Valero, J.A. Riancho, Diverging results of areal and volumetric bone mineral density in Down syndrome. Osteoporos. Int. 28(3), 965–972 (2017). CrossRefGoogle Scholar
  17. 17.
    B.C. Silva, M.D. Walker, A. Abraham, S. Boutroy, C. Zhang, D.J. McMahon, G. Liu, D. Hans, J.P. Bilezikian, Trabecular bone score is associated with volumetric bone density and microarchitecture as assessed by central QCT and HRpQCT in Chinese American and white women. J. Clin. Densitom. 16(4), 554–561 (2013)CrossRefGoogle Scholar
  18. 18.
    IBGE: Instituto Brasileiro de Geografia e Estatística, Ministério da Saúde, Brasil. 2008–2009. Accessed 6 June 2019.
  19. 19.
    WHO: WHO Growth reference data for children and adolescents. Accessed 6 June 2019.
  20. 20.
    W. Leslie, E. Shevroja, H. Johansson, E. McCloskey, N. Harvey, J. Kanis, D. Hans, Risk-equivalent T-score adjustment for using lumbar spine trabecular bone score (TBS): the Manitoba BMD registry. Osteoporos. Int. 29(3), 751–758 (2018)CrossRefGoogle Scholar
  21. 21.
    S.R. Cummings, M.C. Nevitt, W.S. Browner, K. Stone, K.M. Fox, K.E. Ensrud, J. Cauley, D. Black, T.M. Vogt, Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. New Engl. J. Med. 332(12), 767–773 (1995). CrossRefGoogle Scholar
  22. 22.
    M. Gunnes, E.H. Lehmann, D. Mellstrom, O. Johnell, The relationship between anthropometric measurements and fractures in women. Bone 19(4), 407–413 (1996)CrossRefGoogle Scholar
  23. 23.
    D. Hemenway, D. Feskanich, G.A. Colditz, Body height and hip fracture: a cohort study of 90,000 women. Int. J. Epidemiol. 24(4), 783–786 (1995)CrossRefGoogle Scholar
  24. 24.
    A. Bjornerem, Q.M. Bui, A. Ghasem-Zadeh, J.L. Hopper, R. Zebaze, E. Seeman, Fracture risk and height: an association partly accounted for by cortical porosity of relatively thinner cortices. J. Bone Miner. Res. 28(9), 2017–2026 (2013). CrossRefGoogle Scholar
  25. 25.
    D. Xiaoge, L. Eryuan, W. Xianping, Z. Zhiguang, H. Gan, J. Zaijing, P. Xiaoli, T. Hongzhuan, W. Hanwen, Bone mineral density differences at the femoral neck and Ward’s triangle: a comparison study on the reference data between Chinese and Caucasian women. Calcif. Tissue Int. 67(3), 195–198 (2000)CrossRefGoogle Scholar
  26. 26.
    D.S. Lauderdale, S.J. Jacobsen, S.E. Furner, P.S. Levy, J.A. Brody, J. Goldberg, Hip fracture incidence among elderly Asian-American populations. Am. J. Epidemiol. 146(6), 502–509 (1997)CrossRefGoogle Scholar
  27. 27.
    X. Ling, L. Aimin, Z. Xihe, C. Xiaoshu, S.R. Cummings, Very low rates of hip fracture in Beijing, People’s Republic of China: the Beijing Osteoporosis Project. Am. J. Epidemiol. 144(9), 901–907 (1996)CrossRefGoogle Scholar
  28. 28.
    M.D. Walker, D.J. McMahon, J. Udesky, G. Liu, J.P. Bilezikian, Application of high‐resolution skeletal imaging to measurements of volumetric BMD and skeletal microarchitecture in Chinese‐American and white women: explanation of a paradox. J. Bone Miner. Res. 24(12), 1953–1959 (2009)CrossRefGoogle Scholar
  29. 29.
    M.D. Walker, X.S. Liu, E. Stein, B. Zhou, E. Bezati, D.J. McMahon, J. Udesky, G. Liu, E. Shane, X.E. Guo, Differences in bone microarchitecture between postmenopausal Chinese‐American and white women. J. Bone Miner. Res. 26(7), 1392–1398 (2011)CrossRefGoogle Scholar
  30. 30.
    N. Crabtree, W. Högler, M. Cooper, N. Shaw, Diagnostic evaluation of bone densitometric size adjustment techniques in children with and without low trauma fractures. Osteoporos. Int. 24(7), 2015–2024 (2013)CrossRefGoogle Scholar
  31. 31.
    B.C. Silva, S.B. Broy, S. Boutroy, J.T. Schousboe, J.A. Shepherd, W.D. Leslie, 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 (2015). CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Pedro Paulo Martins Alvarenga
    • 1
    • 2
  • Barbara Campolina Silva
    • 1
    • 3
    • 4
    Email author
  • Mariana Picoli Diniz
    • 1
  • Milena Bellei Leite
    • 1
  • Caroline Alves Moreira da Silva
    • 1
  • Jessica de Cássia Mendes Eleutério
    • 1
  • Maria Marta Sarquis Soares
    • 2
    • 3
  • John P. Bilezikian
    • 5
  • Bruno Muzzi Camargos
    • 6
  1. 1.School of MedicineCentro Universitário de Belo Horizonte – UNI-BHBelo HorizonteBrazil
  2. 2.Department of MedicineFederal University of Minas Gerais – UFMG –Belo HorizonteBrazil
  3. 3.Division of Endocrinology, Hospital Felicio RochoBelo HorizonteBrazil
  4. 4.Division of Endocrinology, Santa Casa de Belo HorizonteBelo HorizonteBrazil
  5. 5.Metabolic Bone Diseases Unit, Division of Endocrinology, Department of Medicine, College of Physicians and SurgeonsColumbia UniversityNew YorkUSA
  6. 6.Centro de Densitometria Óssea/Hospital Mater DeiBelo HorizonteBrazil

Personalised recommendations