Trabecular Bone Score: A Noninvasive Analytical Method Based Upon the DXA Image

The trabecular bone score (TBS) is a gray‐level textural metric that can be extracted from the two‐dimensional lumbar spine dual‐energy X‐ray absorptiometry (DXA) image. TBS is related to bone microarchitecture and provides skeletal information that is not captured from the standard bone mineral density (BMD) measurement. Based on experimental variograms of the projected DXA image, TBS has the potential to discern differences between DXA scans that show similar BMD measurements. An elevated TBS value correlates with better skeletal microstructure; a low TBS value correlates with weaker skeletal microstructure. Lumbar spine TBS has been evaluated in cross‐sectional and longitudinal studies. The following conclusions are based upon publications reviewed in this article: 1) TBS gives lower values in postmenopausal women and in men with previous fragility fractures than their nonfractured counterparts; 2) TBS is complementary to data available by lumbar spine DXA measurements; 3) TBS results are lower in women who have sustained a fragility fracture but in whom DXA does not indicate osteoporosis or even osteopenia; 4) TBS predicts fracture risk as well as lumbar spine BMD measurements in postmenopausal women; 5) efficacious therapies for osteoporosis differ in the extent to which they influence the TBS; 6) TBS is associated with fracture risk in individuals with conditions related to reduced bone mass or bone quality. Based on these data, lumbar spine TBS holds promise as an emerging technology that could well become a valuable clinical tool in the diagnosis of osteoporosis and in fracture risk assessment. © 2014 American Society for Bone and Mineral Research.

[1]  D. Hans,et al.  The OsteoLaus Cohort Study , 2012, Osteologie.

[2]  C. Roux,et al.  Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. , 2012, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[3]  Ammar Sarwar,et al.  Distal radius in adolescent girls with anorexia nervosa: trabecular structure analysis with high-resolution flat-panel volume CT. , 2008, Radiology.

[4]  Daniel Chappard,et al.  Texture analysis of X-ray radiographs is correlated with bone histomorphometry , 2004, Journal of Bone and Mineral Metabolism.

[5]  J. Aaron,et al.  The microanatomy of trabecular bone loss in normal aging men and women. , 1987, Clinical orthopaedics and related research.

[6]  D. Hans,et al.  Trabecular bone score improves fracture risk prediction in non-osteoporotic women: the OFELY study , 2012, Osteoporosis International.

[7]  F. Fayad,et al.  Influence of age, morphological characteristics, and lumbar spine bone mineral density on lumbar spine trabecular bone score in Lebanese women. , 2014, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[8]  S. Bonnick Bone Densitometry in Clinical Practice: Application and Interpretation , 2003 .

[9]  O Johnell,et al.  A family history of fracture and fracture risk: a meta-analysis. , 2004, Bone.

[10]  Jacques P. Brown,et al.  The use of clinical risk factors enhances the performance of BMD in the prediction of hip and osteoporotic fractures in men and women , 2007, Osteoporosis International.

[11]  Koichi Ogawa,et al.  Analysis of trabecular patterns using fractal dimensions , 1995, 1995 IEEE Nuclear Science Symposium and Medical Imaging Conference Record.

[12]  I. Chiodini,et al.  Bone quality, as measured by trabecular bone score in patients with adrenal incidentalomas with and without subclinical hypercortisolism , 2012, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[13]  R. Winzenrieth,et al.  Is bone microarchitecture status of the lumbar spine assessed by TBS related to femoral neck fracture? A Spanish case–control study , 2013, Osteoporosis International.

[14]  P. Levitz,et al.  Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects , 2012, Osteoporosis International.

[15]  Harry K. Genant,et al.  Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. , 1993, The American journal of medicine.

[16]  Laurent Pothuaud,et al.  Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. , 2008, Bone.

[17]  J. Kaufman,et al.  In postmenopausal women with osteoporosis, denosumab significantly improved trabecular bone score (TBS), an index of trabecular microarchitecture , 2012 .

[18]  S. Majumdar,et al.  Current diagnostic techniques in the evaluation of bone architecture , 2004, Current osteoporosis reports.

[19]  M. Giger,et al.  Radiographic texture analysis of densitometer-generated calcaneus images differentiates postmenopausal women with and without fractures , 2006, Osteoporosis International.

[20]  Peter E. Undrill,et al.  Identification of hip fracture patients from radiographs using Fourier analysis of the trabecular structure: a cross-sectional study , 2004, BMC Medical Imaging.

[21]  D. Hans,et al.  Effects of Exemestane and Tamoxifen treatment on bone texture analysis assessed by TBS in comparison with bone mineral density assessed by DXA in women with breast cancer. , 2014, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[22]  C. Slemenda,et al.  Age and bone mass as predictors of fracture in a prospective study. , 1988, The Journal of clinical investigation.

[23]  M. Iki,et al.  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 , 2014, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[24]  L. Pothuaud,et al.  Evaluation of the potential use of trabecular bone score to complement bone mineral density in the diagnosis of osteoporosis: a preliminary spine BMD-matched, case-control study. , 2009, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[25]  S. Khosla Update in male osteoporosis. , 2010, The Journal of clinical endocrinology and metabolism.

[26]  O Johnell,et al.  A meta-analysis of previous fracture and subsequent fracture risk. , 2004, Bone.

[27]  A. Silman,et al.  Predictive Value of BMD for Hip and Other Fractures , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[28]  J. Bilezikian,et al.  Trabecular bone score is associated with volumetric bone density and microarchitecture as assessed by central QCT and HRpQCT in Chinese American and white women. , 2013, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[29]  D. Felsenberg,et al.  Added value of trabecular bone score to bone mineral density for prediction of osteoporotic fractures in postmenopausal women: the OPUS study. , 2013, Bone.

[30]  S. Cummings,et al.  Mortality following fractures in older women. The study of osteoporotic fractures. , 1997, Archives of internal medicine.

[31]  Renaud Winzenrieth,et al.  Three-dimensional (3D) microarchitecture correlations with 2D projection image gray-level variations assessed by trabecular bone score using high-resolution computed tomographic acquisitions: effects of resolution and noise. , 2013, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[32]  C. Cooper,et al.  Epidemiology of osteoporosis. , 2002, Best practice & research. Clinical rheumatology.

[33]  C. Rubin Emerging concepts in osteoporosis and bone strength , 2005, Current medical research and opinion.

[34]  Sharmila Majumdar,et al.  In vivo ultra‐high‐field magnetic resonance imaging of trabecular bone microarchitecture at 7 T , 2008, Journal of magnetic resonance imaging : JMRI.

[35]  D. Hans,et al.  Effects of zoledronate versus placebo on spine bone mineral density and microarchitecture assessed by the trabecular bone score in postmenopausal women with osteoporosis: A three‐year study , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[36]  S. Majumdar,et al.  Fractal geometry and vertebral compression fractures , 1994, Journal of Bone and Mineral Research.

[37]  Laurent Pothuaud,et al.  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. , 2011, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[38]  Ann L Oberg,et al.  Effects of Sex and Age on Bone Microstructure at the Ultradistal Radius: A Population‐Based Noninvasive In Vivo Assessment , 2005, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[39]  D. Bauer,et al.  Assessment of vertebral fracture using densitometric morphometry. , 2005, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[40]  M. Ito,et al.  Trabecular texture analysis of CT images in the relationship with spinal fracture. , 1995, Radiology.

[41]  D. Courteix,et al.  Fractal analysis of bone texture: a screening tool for stress fracture risk? , 2004, European journal of clinical investigation.

[42]  M. H. Bedoui,et al.  On the Relations Between 2D and 3D Fractal Dimensions: Theoretical Approach and Clinical Application in Bone Imaging , 2008 .

[43]  D. Hans,et al.  A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. , 2010, Bone.

[44]  D. Hans,et al.  Generation and validation of a normative, age-specific reference curve for lumbar spine trabecular bone score (TBS) in French women , 2013, Osteoporosis International.

[45]  E. Romagnoli,et al.  "Trabecular Bone Score" (TBS): an indirect measure of bone micro-architecture in postmenopausal patients with primary hyperparathyroidism. , 2013, Bone.

[46]  D. Hans,et al.  Die OsteoLaus-Kohortenstudie – Die Kombination aus Knochenmineraldichte, Mikroarchitektur-Score und Wirbelfrakturerkennung, abgeleitet aus einer einzelnen DXA-Aufnahme, und klinischen Risikofaktoren verbessert deutlich die Identifizierung von Frauen mit hohem Frakturrisiko , 2012 .

[47]  Claus Christiansen,et al.  Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. , 1994, World Health Organization technical report series.

[48]  M. Bouxsein,et al.  The predictive value of trabecular bone score (TBS) on whole lumbar vertebrae mechanics: an ex vivo study , 2013, Osteoporosis International.

[49]  R. Eastell,et al.  Bone mineral density and bone turnover in spinal osteoarthrosis. , 1995, Annals of the rheumatic diseases.

[50]  M. Giger,et al.  Computerized radiographic analysis of osteoporosis: preliminary evaluation. , 1993, Radiology.

[51]  H. K. Genant,et al.  Advanced CT bone imaging in osteoporosis , 2008, Rheumatology.

[52]  Christian M. Langton,et al.  Comparison of 3D finite element analysis derived stiffness and BMD to determine the failure load of the excised proximal femur. , 2009, Medical engineering & physics.

[53]  C C Glüer,et al.  Simple measurement of femoral geometry predicts hip fracture: The study of osteoporotic fractures , 1993, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[54]  D. Hans,et al.  Vertebral microarchitecture and fragility fracture in men: a TBS study. , 2014, Bone.

[55]  Olof Johnell,et al.  A Meta‐Analysis of Prior Corticosteroid Use and Fracture Risk , 2004, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[56]  A. Tosteson,et al.  Incidence and Economic Burden of Osteoporosis‐Related Fractures in the United States, 2005–2025 , 2007, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[57]  P. Delmas,et al.  Independent predictors of all osteoporosis-related fractures in healthy postmenopausal women: the OFELY study. , 2003, Bone.

[58]  M. Nevitt,et al.  Vertebral fracture assessment using a semiquantitative technique , 1993, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[59]  J. Eisman,et al.  Femoral Neck Axis Length, Height Loss and Risk of Hip Fracture in Males and Females , 1998, Osteoporosis International.

[60]  W. Leslie,et al.  TBS (trabecular bone score) and diabetes-related fracture risk. , 2013, The Journal of clinical endocrinology and metabolism.

[61]  M. Bouxsein,et al.  In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. , 2005, The Journal of clinical endocrinology and metabolism.

[62]  S. Cremers,et al.  Trabecular bone score (TBS)--a novel method to evaluate bone microarchitectural texture in patients with primary hyperparathyroidism. , 2013, The Journal of clinical endocrinology and metabolism.

[63]  N. Ghannam,et al.  Book review: Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. , 1994, Annals of Saudi medicine.

[64]  E L Hannan,et al.  Mortality and locomotion 6 months after hospitalization for hip fracture: risk factors and risk-adjusted hospital outcomes. , 2001, JAMA.

[65]  M. Reiser,et al.  Differentiation between post-menopausal women with and without hip fractures: enhanced evaluation of clinical DXA by topological analysis of the mineral distribution in the scan images , 2007, Osteoporosis International.

[66]  M. DePalma,et al.  Spine Osteoarthritis , 2012, PM & R : the journal of injury, function, and rehabilitation.

[67]  A. Hofman,et al.  Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. , 2005, Osteoporosis International.

[68]  W. Leslie,et al.  Effects of anti-resorptive agents on trabecular bone score (TBS) in older women , 2013, Osteoporosis International.

[69]  J. Kanis,et al.  Adjustment of FRAX probability according to lumbar spine Trabecular Bone Score (TBS): The Manitoba BMD Cohort , 2013 .

[70]  O. Johnell,et al.  An estimate of the worldwide prevalence and disability associated with osteoporotic fractures , 2006, Osteoporosis International.

[71]  E. Barrett-Connor,et al.  Prediction of Fracture Risk in Postmenopausal White Women With Peripheral Bone Densitometry: Evidence From the National Osteoporosis Risk Assessment , 2002, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[72]  R. Eastell,et al.  Use of DXA‐based finite element analysis of the proximal femur in a longitudinal study of hip fracture , 2013, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[73]  W. Leslie,et al.  Clinical factors associated with trabecular bone score. , 2013, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[74]  J. Cauley,et al.  Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. , 2005, Archives of internal medicine.

[75]  P. Levitz,et al.  Fractal Dimension of Trabecular Bone Projection Texture Is Related to Three‐Dimensional Microarchitecture , 2000, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[76]  C. Cooper,et al.  European guidance for the diagnosis and management of osteoporosis in postmenopausal women , 2008, Osteoporosis International.

[77]  D. Hans,et al.  Spine trabecular bone score subsequent to bone mineral density improves fracture discrimination in women. , 2014, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[78]  L. Pothuaud,et al.  A Retrospective Case–Control Study Assessing the Role of Trabecular Bone Score in Postmenopausal Caucasian Women with Osteopenia: Analyzing the Odds of Vertebral Fracture , 2010, Calcified Tissue International.

[79]  Eugene V. McCloskey,et al.  Assessing the Impact of Osteoporosis on the Burden of Hip Fractures , 2012, Calcified Tissue International.

[80]  I. Chiodini,et al.  Bone quality, as measured by trabecular bone score, in patients with primary hyperparathyroidism. , 2013, European journal of endocrinology.

[81]  Raj Acharya,et al.  Analysis of bone X-rays using morphological fractals , 1993, IEEE Trans. Medical Imaging.

[82]  W. Leslie,et al.  Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: The manitoba study , 2011, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[83]  R. Eastell,et al.  Use of DXA‐Based Structural Engineering Models of the Proximal Femur to Discriminate Hip Fracture , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.