Original ArticleCorrelations 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
Introduction
Osteoporosis is a skeletal disorder characterized by compromised bone strength, which predisposes an affected individual to bone fractures (1). The management of osteoporosis requires accurate clinical assessments of bone strength and fracture risk. Dual-energy X-ray absorptiometry (DXA) is commonly used to diagnose osteoporosis in clinical practice, providing accurate estimates of bone mass through the evaluation of bone mineral density (BMD). However, BMD is not always an accurate predictor of fracture risk 2, 3, 4, 5. One reason may be that bone mass is not the only contributor to bone strength. Consequently, evaluating some other bone parameter, such as bone microarchitecture, could significantly enhance the assessment of bone strength 6, 7, 8 and fracture risk.
In recent years, a number of developments have contributed to bone microarchitecture assessment techniques. Among the noninvasive techniques, (peripheral) quantitative computed tomography (9) and magnetic resonance imaging (10) allow for the direct or indirect measurement of bone microarchitecture, and both have benefited from significant enhancements in acquisition technology and/or image analysis. Nonetheless, these two techniques remain impractical for the routine screening and clinical management of osteoporosis because of high costs, patient inconvenience, and their availability for such diseases. Histomorphometric assessment of iliac crest bone biopsies remains the gold-standard method for the direct assessment of bone microarchitecture, but this technique is invasive and not directly 3 dimensional (3D). A major challenge, therefore, has been to develop some novel technique that allows for the efficient, noninvasive clinical evaluation of bone microarchitecture status. 2D X-ray-based images, such as plain radiographs, have been investigated widely as a more practical alternative for the noninvasive and indirect assessment of bone microarchitecture. Different gray-level features have been explored, including fractal dimension and Fourier analysis, among others 11, 12, 13, 14, 15, 16.
Over the past several years, DXA technology has advanced dramatically, in terms of both its hardware and software components (17). Recent generations of DXA systems provide not only accurate and reproducible measurements of BMD but also the opportunity to use high-quality DXA scans in place of standard X-rays to confirm and characterize existing vertebral fractures. Hence, Genant et al's (18) indices of vertebral fracture (19) and certain indices related to hip geometry 20, 21 can be evaluated directly from high-quality DXA images. More recently, a new application called hip structure/hip strength analysis allows us to obtain information related to bone strength of the proximal femur 22, 23. These macroscopic geometrical measurements constitute risk factors that are independent of BMD, and the ability to obtain them from the same DXA examination is an additional advantage. Langton et al (24) have developed a new technique, called finite element analysis of X-ray images (FEXI), which uses a finite element analysis model applied to DXA gray-level images. This technique permits the evaluation of a new DXA-based measure: “FEXI stiffness.” Boehm et al (25) introduced an algorithm to evaluate the hip DXA scans using quantitative image analysis procedures based on Minkowski Functionals. This new DXA-based measure considers bone mineral distribution in the proximal femur, instead of just BMD, and may be well suited to enhance standard densitometric evaluations as a predictor of hip fracture risk.
Trabecular bone score (TBS) is a new gray-level texture measurement that can be applied to DXA images (24). TBS is based on the measurement of the experimental variogram derived from a gray-level DXA image. In previous studies, we identified significant correlations between TBS—as evaluated from simulated 2D-projection micro-computed tomography (μ-CT) images—and standard 3D parameters of bone microarchitecture—evaluated using high-resolution μ-CT reconstructions—in sets of human vertebral bone pieces (26). At 93-μm plane resolution, strong significant correlations have been obtained between TBS and Parfitt's microarchitecture parameters, such as connectivity density (connD: 0.856 ≤ r ≤ 0.862, p < 0.001); trabecular number (TbN: 0.805 ≤ r ≤ 0.810, p < 0.001); and trabecular spacing (TbSp: −0.714 ≤ r ≤ −0.726, p < 0.001), regardless of the X-ray energy used for the projection (26). On the other hand, the effects of image resolution degradation (from 93- to 1488-μm plane resolution) and noise have been studied (27) using μ-CT images. Significant correlations were obtained between TBS and 3D microarchitecture parameters, regardless of image resolution, up to a certain level. Strong correlations were obtained with connD (0.843 ≤ r ≤ 0.867), TbN (0.764 ≤ r ≤ 0.805), and TbSp (−0.701 ≤ r ≤ −0.638), and with those up to a resolution of 744 μm. From a clinical point of view, several cross-sectional studies have shown the ability of TBS to discriminate subjects with vertebral fractures from healthy subjects matched for age, BMD, or both 28, 29, 30. It has also been demonstrated that TBS is relevant in secondary osteoporosis 31, 32, 33. Finally, it has been shown that spine TBS predicts major osteoporotic fractures as well as, and independent of, spine BMD, and that combining the TBS microarchitecture index with BMD from conventional DXA incrementally improves fracture predictions in postmenopausal women 34, 35.
The main objective of the present study was to determine whether the 2D/3D correlations previously identified during the feasibility study could be reproduced when TBS of anteroposterior (AP) DXA images are considered.
Section snippets
Human Cadaver Vertebrae
Thirty human cadaver lumbar vertebrae were obtained from the Anatomy Laboratory at the University Hospital of Bordeaux (France). These dried bone pieces were free of bone marrow, in accordance with standard procedures. Whole vertebrae (an intact segment of the spine including the superimposing posterior elements) were considered in this study. In addition, these vertebrae were protected using a thin layer of epoxy resin. It has been verified that this thin layer has no effect on CT or DXA
Descriptive Statistics
The values of TBS varied from 1.055 to 1.511 (Table 1), and the analysis of TBS value distribution failed to identify any outliers. BMD values ranged from 0.817 to 1.568 g/cm2 (Table 1), again without any evidence of outliers. Hence, the data set of the study, derived from 30 human cadaver vertebrae, appeared to be representative of routine clinical values for TBS and BMD. Analysis of the distribution for the various 3D bone microarchitecture parameters again failed to reveal any outliers.
Trabecular Bone Score Reproducibility Evaluation
From
Discussion
TBS was significantly correlated with the 3D parameters of bone microarchitecture, and this was mostly independent of any association with BMD. The highest degree of correlation was apparent between TBS and connD, with TBS explaining 67.2% of the variance in 3D connectivity. The relationship between TBS and 3D bone microarchitecture parameters was such that a low TBS was indicative of weak or degraded microarchitecture, associated with low connectivity, high TbSp, and a reduced number of
Acknowledgments
Sincere thanks to all personnel in the Anatomy Laboratory at the University Hospital of Bordeaux who assisted with the bone samples: Professors Dominique Midy and Jean-Marc Vital; Drs Benoît Lavignolle and Mathieu de Sèze; and Mr Jean-Jacques Barbouteau, Mr Etienne Delamarre, and Mr José Prata. Special thanks also to Aurelie Bergey for the DXA and μ-CT acquisitions. Finally, the authors want to thank Dr Alain Heraud, who granted them access to his Prodigy Device, and Kevin White from Science
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