Semin Musculoskelet Radiol 2024; 28(05): 539-546
DOI: 10.1055/s-0044-1788886
Review Article

Trabecular Bone Score to Enhance Fracture Risk Prediction and Treatment Strategies in Osteoporosis

Guillaume Gatineau
1   Bone and Joint Department, Lausanne University Hospital, Lausanne, Switzerland
,
Didier Hans
1   Bone and Joint Department, Lausanne University Hospital, Lausanne, Switzerland
,
Karen Hind
2   Wolfson Research Institute of Health and Wellbeing, Durham University, Durham, United Kingdom
3   Medical School, Lancaster University, Lancaster, United Kingdom
› Author Affiliations

Abstract

The Trabecular Bone Score (TBS), a gray-level textural assessment derived from dual-energy X-ray absorptiometry images, serves as a validated index of trabecular bone microarchitecture. Over the past decade, significant evidence has highlighted the usefulness of TBS in primary and secondary osteoporosis, leading to its integration with the Fracture Risk Assessment Tool (FRAX) and bone mineral density (BMD) T-score adjustments. This review explores the role of TBS in fracture prediction, treatment initiation, and monitoring. Studies confirm that TBS enhances fracture risk prediction in both primary and secondary osteoporosis when combined with BMD and clinical risk factors. Evidence also suggests that including TBS alongside BMD and FRAX offers significant potential for treatment stratification, considering the overall skeletal profile, such as bone mass, bone quality, and clinical risk factors. Consequently, TBS has become a standard part of clinical care worldwide. Future enhancements hope to adjust for soft tissue thickness, broadening the applicability of TBS across diverse body types and pediatric populations.



Publication History

Article published online:
15 October 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Peck WA. Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. Am J Med 1993; 94 (06) 646-650
  • 2 Siris ES, Miller PD, Barrett-Connor E. et al. Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women: results from the National Osteoporosis Risk Assessment. JAMA 2001; 286 (22) 2815-2822
  • 3 Binkley N, Morin SN, Martineau P, Lix LM, Hans D, Leslie WD. Frequency of normal bone measurement in postmenopausal women with fracture: a registry-based cohort study. Osteoporos Int 2020; 31 (12) 2337-2344
  • 4 Pothuaud L, Carceller P, Hans D. Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone 2008; 42 (04) 775-787
  • 5 Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA. 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 2011; 14 (03) 302-312
  • 6 Muschitz C, Kocijan R, Haschka J. et al. TBS reflects trabecular microarchitecture in premenopausal women and men with idiopathic osteoporosis and low-traumatic fractures. Bone 2015; 79: 259-266
  • 7 Shevroja E, Reginster JY, Lamy O. et al. Update on the clinical use of trabecular bone score (TBS) in the management of osteoporosis: results of an expert group meeting organized by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO), and the International Osteoporosis Foundation (IOF) under the auspices of WHO Collaborating Center for Epidemiology of Musculoskeletal Health and Aging. Osteoporos Int 2023; 34 (09) 1501-1529
  • 8 McCloskey EV, Odén A, Harvey NC. et al. A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 2016; 31 (05) 940-948
  • 9 Tamaki J, Iki M, Sato Y, Winzenrieth R, Kajita E, Kagamimori S. JPOS Study Group. Does Trabecular Bone Score (TBS) improve the predictive ability of FRAX® for major osteoporotic fractures according to the Japanese Population-Based Osteoporosis (JPOS) cohort study?. J Bone Miner Metab 2019; 37 (01) 161-170
  • 10 Iki M, Fujita Y, Tamaki J. et al. Trabecular bone score may improve FRAX® prediction accuracy for major osteoporotic fractures in elderly Japanese men: the Fujiwara-kyo Osteoporosis Risk in Men (FORMEN) Cohort Study. Osteoporos Int 2015; 26 (06) 1841-1848
  • 11 Schousboe JT, Vo T, Taylor BC. et al; Osteoporotic Fractures in Men MrOS Study Research Group. 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 2016; 31 (03) 690-697
  • 12 Martineau P, Leslie WD, Johansson H. et al. In which patients does lumbar spine trabecular bone score (TBS) have the largest effect?. Bone 2018; 113: 161-168
  • 13 Leslie WD, Shevroja E, Johansson H. et al. Risk-equivalent T-score adjustment for using lumbar spine trabecular bone score (TBS): the Manitoba BMD registry. Osteoporos Int 2018; 29 (03) 751-758
  • 14 Popp AW, Meer S, Krieg MA, Perrelet R, Hans D, Lippuner K. Bone mineral density (BMD) and vertebral trabecular bone score (TBS) for the identification of elderly women at high risk for fracture: the SEMOF cohort study. Eur Spine J 2016; 25 (11) 3432-3438
  • 15 Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM. Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 2014; 25 (07) 1969-1973
  • 16 Kim JH, Choi HJ, Ku EJ. et al. Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab 2015; 100 (02) 475-482
  • 17 Tang SY, Zeenath U, Vashishth D. Effects of non-enzymatic glycation on cancellous bone fragility. Bone 2007; 40 (04) 1144-1151
  • 18 Jackuliak P, Kužma M, Killinger Z, Payer J. Good long-term glycemic compensation is associated with better trabecular bone score in postmenopausal women with type 2 diabetes. Physiol Res 2019; 68 (Suppl. 02) S149-S156
  • 19 Leslie WD, Aubry-Rozier B, Lix LM, Morin SN, Majumdar SR, Hans D. Spine bone texture assessed by trabecular bone score (TBS) predicts osteoporotic fractures in men: the Manitoba Bone Density Program. Bone 2014; 67: 10-14
  • 20 Choi YJ, Ock SY, Chung YS. 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 2016; 19 (04) 507-514
  • 21 Bonaccorsi G, Fila E, Messina C. et al. Comparison of trabecular bone score and hip structural analysis with FRAX® in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res 2017; 29 (05) 951-957
  • 22 Lin YC, Wu J, Kuo SF. et al. Vertebral fractures in type 2 diabetes patients: utility of trabecular bone score and relationship with serum bone turnover biomarkers. J Clin Densitom 2020; 23 (01) 37-43
  • 23 Paul J, Devarapalli V, Johnson JT. et al. 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. Osteoporos Int 2021; 32 (08) 1585-1593
  • 24 Belaya ZE, Hans D, Rozhinskaya LY. et al. The risk factors for fractures and trabecular bone-score value in patients with endogenous Cushing's syndrome. Arch Osteoporos 2015; 10: 44
  • 25 Paggiosi MA, Peel NFA, Eastell R. The impact of glucocorticoid therapy on trabecular bone score in older women. Osteoporos Int 2015; 26 (06) 1773-1780
  • 26 Lee KA, Kim J, Kim HJ, Kim HS. Discriminative ability of trabecular bone score over bone mineral density for vertebral and fragility fracture in patients treated with long-term and low-dose glucocorticoid. Int J Rheum Dis 2021; 24 (08) 1053-1060
  • 27 Naylor KL, Prior J, Garg AX. et al. Trabecular bone score and incident fragility fracture risk in adults with reduced kidney function. Clin J Am Soc Nephrol 2016; 11 (11) 2032-2040
  • 28 Catalano A, Gaudio A, Bellone F. et al. Trabecular bone score and phalangeal quantitative ultrasound are associated with muscle strength and fracture risk in hemodialysis patients. Front Endocrinol (Lausanne) 2022; 13: 940040
  • 29 Kim D, Cho SK, Kim JY, Choi YY, Sung YK. Association between trabecular bone score and risk factors for fractures in Korean female patients with rheumatoid arthritis. Mod Rheumatol 2016; 26 (04) 540-545
  • 30 Choi YJ, Chung YS, Suh CH, Jung JY, Kim HA. Trabecular bone score as a supplementary tool for the discrimination of osteoporotic fractures in postmenopausal women with rheumatoid arthritis. Medicine (Baltimore) 2017; 96 (45) e8661
  • 31 Kang KY, Kim IJ, Park SH, Hong YS. Associations between trabecular bone score and vertebral fractures in patients with axial spondyloarthritis. Rheumatology (Oxford) 2018; 57 (06) 1033-1040
  • 32 Richards C, Hans D, Leslie WD. Trabecular bone score (TBS) predicts fracture in ankylosing spondylitis: the Manitoba BMD registry. J Clin Densitom 2020; 23 (04) 543-548
  • 33 Kim HA, Lee HY, Jung JY, Suh CH, Chung YS, Choi YJ. Trabecular bone score is a useful parameter for the prediction of vertebral fractures in patients with polymyalgia rheumatica. J Clin Densitom 2020; 23 (03) 373-380
  • 34 Lai EL, Huang WN, Chen HH. et al. Degraded microarchitecture by low trabecular bone score is associated with prevalent vertebral fractures in patients with systemic lupus erythematosus. Arch Osteoporos 2020; 15 (01) 54
  • 35 Lee KA, Kim HJ, Kim HS. Comparison of predictive value of FRAX, trabecular bone score, and bone mineral density for vertebral fractures in systemic sclerosis: a cross-sectional study. Medicine (Baltimore) 2023; 102 (02) e32580
  • 36 Ciullini L, Pennica A, Argento G. et al. Trabecular bone score (TBS) is associated with sub-clinical vertebral fractures in HIV-infected patients. J Bone Miner Metab 2018; 36 (01) 111-118
  • 37 Kužma M, Vaňuga P, Ságová I. et al. Non-invasive DXA-derived bone structure assessment of acromegaly patients: a cross-sectional study. Eur J Endocrinol 2019; 180 (03) 201-211
  • 38 Sakane EN, Vieira MCC, Lazaretti-Castro M, Maeda SS. Predictors of poor bone microarchitecture assessed by trabecular bone score in postsurgical hypoparathyroidism. J Clin Endocrinol Metab 2019; 104 (12) 5795-5803
  • 39 Jones AR, Simons K, Harvey S, Grill V. Bone mineral density compared to trabecular bone score in primary hyperparathyroidism. J Clin Med 2022; 11 (02) 330
  • 40 Ogiso Y, Hanai T, Nishimura K. et al. Usefulness of the trabecular bone score in assessing the risk of vertebral fractures in patients with cirrhosis. J Clin Med 2022; 11 (06) 1562
  • 41 Baron R, Ferrari S, Russell RGG. Denosumab and bisphosphonates: different mechanisms of action and effects. Bone 2011; 48 (04) 677-692
  • 42 Di Gregorio S, Del Rio L, Rodriguez-Tolra J, Bonel E, García M, Winzenrieth R. Comparison between different bone treatments on areal bone mineral density (aBMD) and bone microarchitectural texture as assessed by the trabecular bone score (TBS). Bone 2015; 75: 138-143
  • 43 Shin MS, Cho EH, Kim HY. Longitudinal change in trabecular bone score during and after treatment of osteoporosis in postmenopausal Korean women. J Bone Metab 2017; 24 (02) 117-124
  • 44 Sooragonda B, Cherian KE, Jebasingh FK. et al. Longitudinal changes in bone mineral density and trabecular bone score following yearly zoledronic acid infusion in postmenopausal osteoporosis—a retrospective-prospective study from southern India. Arch Osteoporos 2019; 14 (01) 79
  • 45 Kim J, Kim KM, Lim S, Kang MI, Baek KH, Min YK. Efficacy of bisphosphonate therapy on postmenopausal osteoporotic women with and without diabetes: a prospective trial. BMC Endocr Disord 2022; 22 (01) 99
  • 46 Kang T, Park SY, Lee SH, Park JH, Suh SW. Comparison of denosumab and zoledronic acid in postmenopausal women with osteoporosis: bone mineral density (BMD) and Trabecular Bone Score (TBS). J Korean Med Sci 2022; 37 (13) e68
  • 47 Hans D, McDermott M, Huang S, Kim M, Shevroja E, McClung M. Long-term effect of denosumab on bone microarchitecture as assessed by tissue thickness-adjusted trabecular bone score in postmenopausal women with osteoporosis: results from FREEDOM and its open-label extension. Osteoporos Int 2023; 34 (06) 1075-1084
  • 48 Leslie WD, Goel H, Binkley N, McCloskey EV, Hans D. Contributions of clinical and technical factors to longitudinal change in Trabecular Bone Score and bone density: a registry-based individual-level analysis. J Bone Miner Res 2023; 38 (04) 512-521
  • 49 Hans D, Shevroja E, McDermott M, Huang S, Kim M, McClung M. Updated trabecular bone score accounting for the soft tissue thickness (TBSTT) demonstrated significantly improved bone microstructure with denosumab in the FREEDOM TBS post hoc analysis. Osteoporos Int 2022; 33 (12) 2517-2525
  • 50 Ferrari SL, Abrahamsen B, Napoli N. et al; Bone and Diabetes Working Group of IOF. Diagnosis and management of bone fragility in diabetes: an emerging challenge. Osteoporos Int 2018; 29 (12) 2585-2596
  • 51 Jiang Y, Zhao JJ, Mitlak BH, Wang O, Genant HK, Eriksen EF. Recombinant human parathyroid hormone (1-34) [teriparatide] improves both cortical and cancellous bone structure. J Bone Miner Res 2003; 18 (11) 1932-1941
  • 52 Bilezikian JP, Hattersley G, Fitzpatrick LA. et al. Abaloparatide-SC improves trabecular microarchitecture as assessed by trabecular bone score (TBS): a 24-week randomized clinical trial. Osteoporos Int 2018; 29 (02) 323-328
  • 53 Cosman F, Hans D, Shevroja E, Wang Y, Mitlak B. Effect of abaloparatide on bone microarchitecture assessed by Trabecular Bone Score in women with osteoporosis: post hoc analysis of ACTIVE and ACTIVExtend. J Bone Miner Res 2023; 38 (04) 464-470
  • 54 Jeong C, Kim J, Lim Y, Ha J, Kang MI, Baek KH. Effect of romosozumab on trabecular bone score compared to anti-resorptive agents in postmenopausal women with osteoporosis. J Bone Metab 2021; 28 (04) 317-323
  • 55 McClung M, Betah D, Leder B. et al. 2022 Effect of romosozumab on bone microarchitecture as assessed by tissue thickness–adjusted Trabecular Bone Score in postmenopausal women with osteoporosis: results from the ARCH study. Paper presented at: Annual Meeting of the American Society for Bone and Mineral Research;. September 9–12, 2022; Austin, TX
  • 56 Curtis EM, Reginster JY, Al-Daghri N. et al. Management of patients at very high risk of osteoporotic fractures through sequential treatments. Aging Clin Exp Res 2022; 34 (04) 695-714
  • 57 Tsai JN, Jiang LA, Lee H, Hans D, Leder BZ. Effects of teriparatide, denosumab, or both on spine trabecular microarchitecture in DATA-switch: a randomized controlled trial. J Clin Densitom 2017; 20 (04) 507-512
  • 58 Pedrazzoni M, Casola A, Verzicco I, Abbate B, Vescovini R, Sansoni P. Longitudinal changes of trabecular bone score after estrogen deprivation: effect of menopause and aromatase inhibition. J Endocrinol Invest 2014; 37 (09) 871-874
  • 59 Hong AR, Kim JH, Lee KH. et al. Long-term effect of aromatase inhibitors on bone microarchitecture and macroarchitecture in non-osteoporotic postmenopausal women with breast cancer. Osteoporos Int 2017; 28 (04) 1413-1422
  • 60 Mariotti V, Page DB, Davydov O. et al. Assessing fracture risk in early stage breast cancer patients treated with aromatase-inhibitors: an enhanced screening approach incorporating trabecular bone score. J Bone Oncol 2016; 7: 32-37
  • 61 Tseng OL, Spinelli JJ, Gotay CC, Ho WY, McBride ML, Dawes MG. Aromatase inhibitors are associated with a higher fracture risk than tamoxifen: a systematic review and meta-analysis. Ther Adv Musculoskelet Dis 2018; 10 (04) 71-90
  • 62 Catalano A, Gaudio A, Agostino RM, Morabito N, Bellone F, Lasco A. Trabecular bone score and quantitative ultrasound measurements in the assessment of bone health in breast cancer survivors assuming aromatase inhibitors. J Endocrinol Invest 2019; 42 (11) 1337-1343
  • 63 Messina OD, Vidal M, Torres JAM. et al. Evidence based Latin American Guidelines of clinical practice on prevention, diagnosis, management and treatment of glucocorticoid induced osteoporosis. A 2022 update: This manuscript has been produced under the auspices of the Committee of National Societies (CNS) and the Committee of Scientific Advisors (CSA) of the International Osteoporosis Foundation (IOF). Aging Clin Exp Res 2022; 34 (11) 2591-2602
  • 64 Chappard D, Legrand E, Basle MF. et al. Altered trabecular architecture induced by corticosteroids: a bone histomorphometric study. J Bone Miner Res 1996; 11 (05) 676-685
  • 65 Dalle Carbonare L, Arlot ME, Chavassieux PM, Roux JP, Portero NR, Meunier PJ. Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis. J Bone Miner Res 2001; 16 (01) 97-103
  • 66 Chuang MH, Chuang TL, Koo M, Wang YF. Trabecular bone score reflects trabecular microarchitecture deterioration and fragility fracture in female adult patients receiving glucocorticoid therapy: a pre-post controlled study. BioMed Res Int 2017; 2017: 4210217
  • 67 Corrado A, Rotondo C, Mele A. et al. Influence of glucocorticoid treatment on trabecular bone score and bone remodeling regulators in early rheumatoid arthritis. Arthritis Res Ther 2021; 23 (01) 180
  • 68 Cauley JA, Ellenberg SS, Schwartz AV, Ensrud KE, Keaveny TM, Snyder PJ. Effect of testosterone treatment on the trabecular bone score in older men with low serum testosterone. Osteoporos Int 2021; 32 (11) 2371-2375
  • 69 Prasad C, Greenspan SL, Vujevich KT. et al. Risedronate may preserve bone microarchitecture in breast cancer survivors on aromatase inhibitors: a randomized, controlled clinical trial. Bone 2016; 90: 123-126
  • 70 Bonani M, Frey D, Graf N, Wüthrich RP. Effect of denosumab on trabecular bone score in de novo kidney transplant recipients. Nephrol Dial Transplant 2019; 34 (10) 1773-1780
  • 71 Dhaliwal R, Hans D, Hattersley G. et al. Abaloparatide in postmenopausal women with osteoporosis and type 2 diabetes: a post hoc analysis of the ACTIVE study. JBMR Plus 2020; 4 (04) e10346
  • 72 Shane E, Shiau S, Recker RR. et al. Denosumab after teriparatide in premenopausal women with idiopathic osteoporosis. J Clin Endocrinol Metab 2022; 107 (04) e1528-e1540
  • 73 Munekawa C, Hashimoto Y, Kitagawa N, Osaka T, Hamaguchi M, Fukui M. Effect of teriparatide on bone mineral density and trabecular bone score in type 2 diabetic patients with osteoporosis: a retrospective cohort study. Medicina (Kaunas) 2022; 58 (04) 481
  • 74 Saag KG, Agnusdei D, Hans D. et al. Trabecular bone score in patients with chronic glucocorticoid therapy–induced osteoporosis treated with alendronate or teriparatide. Arthritis Rheumatol 2016; 68 (09) 2122-2128
  • 75 Shevroja E, Aubry-Rozier B, Hans G. et al. Clinical performance of the updated trabecular bone score (TBS) algorithm, which accounts for the soft tissue thickness: The OsteoLaus study. J Bone Miner Res 2019; 34 (12) 2229-2237
  • 76 Kalkwarf HJ, Shepherd JA, Hans D. et al. Trabecular bone score reference values for children and adolescents according to age, sex, and ancestry. J Bone Miner Res 2022; 37 (04) 776-785