In vitro estimation of fast and slow wave parameters of thin trabecular bone using space-alternating generalized expectation-maximization algorithm

In testing cancellous bone using ultrasound, two types of longitudinal Biot’s waves are observed in the received signal. These are known as fast and slow waves and their appearance depend on the alignment of bone trabeculae in the propagation path and the thickness of the specimen under test (SUT). They can be used as an effective tool for the diagnosis of osteoporosis because wave propagation behavior depends on the bone structure. However, the identification of these waves in the received signal can be difficult to achieve.In this study, ultrasonic wave propagation in a 4 mm thick bovine cancellous bone in the direction parallel to the trabecular alignment is considered. The observed Biot’s fast and slow longitudinal waves are superimposed; which makes it difficult to extract any information from the received signal. These two waves can be separated using the space alternating generalized expectation maximization (SAGE) algorithm. The latter has been used mainly in speech processing.In this new approach, parameters such as, arrival time, center frequency, bandwidth, amplitude, phase and velocity of each wave are estimated. The B-Scan images and its associated A-scans obtained through simulations using Biot’s finite-difference time-domain (FDTD) method are validated experimentally using a thin bone sample obtained from the femoral-head of a 30 months old bovine.     

Ultrasonic pulse waves in cancellous bone analyzed by finite-difference time-domain methods

The trabecular frame of cancellous bone has a high degree of porosity, anisotropy and inhomogeneity. The propagation of ultrasonic waves in cancellous bone is significantly affected by the trabecular structure. In this paper, two two-dimensional finite-difference time-domain (FDTD) methods, which were the popular viscoelastic FDTD method for a viscoelastic medium and Biot's FDTD method for a fluid-saturated porous medium, have been applied to numerically analyze the ultrasonic pulse waves propagating through bovine cancellous bone in the directions parallel and perpendicular to the trabecular alignment. The Biot's fast and slow longitudinal waves, which were identified in previous experiments for the propagation parallel to the trabecular orientation, could be analyzed using Biot's FDTD method rather than the viscoelastic FDTD method. For the single wave propagation in the perpendicular direction, on the other hand, the viscoelastic FDTD result was found to be in more good agreement with the experimental result.     

Ultrasonic characterization of human cancellous bone using the Biot theory: inverse problem

This paper concerns the ultrasonic characterization of human cancellous bone samples by solving the inverse problem using experimental transmitted signals. The ultrasonic propagation in cancellous bone is modeled using the Biot theory modified by the Johnson et al. model for viscous exchange between fluid and structure. The sensitivity of the Young modulus and the Poisson ratio of the skeletal frame is studied showing their effect on the fast and slow wave forms. The inverse problem is solved numerically by the least squares method. Five parameters are inverted: the porosity, tortuosity, viscous characteristic length, Young modulus, and Poisson ratio of the skeletal frame. The minimization of the discrepancy between experiment and theory is made in the time domain. The inverse problem is shown to be well posed, and its solution to be unique. Experimental results for slow and fast waves transmitted through human cancellous bone samples are given and compared with theoretical predictions.     

Determining attenuation properties of interfering fast and slow ultrasonic waves in cancellous bone

Previous studies have shown that interference between fast waves and slow waves can lead to observed negative dispersion in cancellous bone. In this study, the effects of overlapping fast and slow waves on measurements of the apparent attenuation as a function of propagation distance are investigated along with methods of analysis used to determine the attenuation properties. Two methods are applied to simulated data that were generated based on experimentally acquired signals taken from a bovine specimen. The first method uses a time-domain approach that was dictated by constraints imposed by the partial overlap of fast and slow waves. The second method uses a frequency-domain log-spectral subtraction technique on the separated fast and slow waves. Applying the time-domain analysis to the broadband data yields apparent attenuation behavior that is larger in the early stages of propagation and decreases as the wave travels deeper. In contrast, performing frequency-domain analysis on the separated fast waves and slow waves results in attenuation coefficients that are independent of propagation distance. Results suggest that features arising from the analysis of overlapping two-mode data may represent an alternate explanation for the previously reported apparent dependence on propagation distance of the attenuation coefficient of cancellous bone.     

Propagation of two longitudinal waves in a cancellous bone with the closed pore boundary

Ultrasound propagation in cancellous bone (porous media) under the condition of closed pore boundaries was investigated. A cancellous bone and two plate-like cortical bones obtained from a racehorse were prepared. A water-immersion ultrasound technique in the MHz range and a three-dimensional elastic finite-difference time-domain (FDTD) method were used to investigate the waves. The experiments and simulations showed a clear separation of the incident longitudinal wave into fast and slow waves. The findings advance the evaluation of bones based on the two-wave phenomenon for in vivo assessment.     

Influence of cancellous bone microstructure on two ultrasonic wave propagations in bovine femur: an in vitro study

The influence of cancellous bone microstructure on the ultrasonic wave propagation of fast and slow waves was experimentally investigated. Four spherical cancellous bone specimens extracted from two bovine femora were prepared for the estimation of acoustical and structural anisotropies of cancellous bone. In vitro measurements were performed using a PVDF transducer (excited by a single sinusoidal wave at 1 MHz) by rotating the spherical specimens. In addition, the mean intercept length (MIL) and bone volume fraction (BV/TV) were estimated by X-ray micro-computed tomography. Separation of the fast and slow waves was clearly observed in two specimens. The fast wave speed was strongly dependent on the wave propagation direction, with the maximum speed along the main trabecular direction. The fast wave speed increased with the MIL. The slow wave speed, however, was almost constant. The fast wave speeds were statistically higher, and their amplitudes were statistically lower in the case of wave separation than in that of wave overlap.     

Ultrasonic wave propagation in human cancellous bone: application of Biot theory

Ultrasonic wave propagation in human cancellous bone is considered. Reflection and transmission coefficients are derived for a slab of cancellous bone having an elastic frame using Biot's theory modified by the model of Johnson et al. [J. Fluid Mech. 176, 379-402 (1987)] for viscous exchange between fluid and structure. Numerical simulations of transmitted waves in the time domain are worked out by varying the modified Biot parameters. The variation is applied to the governing parameters and is about 20%. From this study, we can gain an insight into the sensitivity of each physical parameter used in this theory. Some parameters play an important role in slow-wave wave form, such as the viscous characteristic length lambda and pore fluid bulk modulus Kf. However, other parameters play an important role in the fast-wave wave form, such as solid density rhos and shear modulus N. We also note from these simulations that some parameters such as porosity phi, tortuosity alpha(infinty), thickness, solid bulk modulus Ks, and skeletal compressibility frame Kb, play an important role simultaneously in both fast and slow wave forms compared to other parameters which act on the wave form of just one of the two waves. The sensitivity of the modified Biot parameters with respect to the transmitted wave depends strongly on the coupling between the solid and fluid phases of the cancellous bone. Experimental results for slow and fast waves transmitted through human cancellous bone samples are given and compared with theoretical predictions.     

Two-wave behavior under various conditions of transition area from cancellous bone to cortical bone

The two-wave phenomenon, the wave separation of a single ultrasonic pulse in cancellous bone, is expected to be a useful tool for the diagnosis of osteoporosis. However, because actual bone has a complicated structure, precise studies on the effect of transition conditions between cortical and cancellous parts are required. This study investigated how the transition condition influenced the two-wave generation using three-dimensional X-ray CT images of an equine radius and a three-dimensional simulation technique. As a result, any changes in the boundary between cortical part and trabecular part, which gives the actual complex structure of bone, did not eliminate the generation of either the primary wave or the secondary wave at least in the condition of clear trabecular alignment. The results led us to the possibility of using the two-wave phenomenon in a diagnostic system for osteoporosis in cases of a complex boundary.     

Inverse problems in cancellous bone: estimation of the ultrasonic properties of fast and slow waves using Bayesian probability theory

Quantitative ultrasonic characterization of cancellous bone can be complicated by artifacts introduced by analyzing acquired data consisting of two propagating waves (a fast wave and a slow wave) as if only one wave were present. Recovering the ultrasonic properties of overlapping fast and slow waves could therefore lead to enhancement of bone quality assessment. The current study uses Bayesian probability theory to estimate phase velocity and normalized broadband ultrasonic attenuation (nBUA) parameters in a model of fast and slow wave propagation. Calculations are carried out using Markov chain Monte Carlo with simulated annealing to approximate the marginal posterior probability densities for parameters in the model. The technique is applied to simulated data, to data acquired on two phantoms capable of generating two waves in acquired signals, and to data acquired on a human femur condyle specimen. The models are in good agreement with both the simulated and experimental data, and the values of the estimated ultrasonic parameters fall within expected ranges.     

The finite element method for micro-scale modeling of ultrasound propagation in cancellous bone

Quantitative ultrasound for bone assessment is based on the correlations between ultrasonic parameters and the properties (mechanical and physical) of cancellous bone. To elucidate the correlations, understanding the physics of ultrasound in cancellous bone is demanded. Micro-scale modeling of ultrasound propagation in cancellous bone using the finite-difference time-domain (FDTD) method has been so far utilized as one of the approaches in this regard. However, the FDTD method accompanies two disadvantages: staircase sampling of cancellous bone by finite difference grids leads to generation of wave artifacts at the solid–fluid interface inside the bone; additionally, this method cannot explicitly satisfy the needed perfect-slip conditions at the interface. To overcome these disadvantages, the finite element method (FEM) is proposed in this study. Three-dimensional finite element models of six water-saturated cancellous bone samples with different bone volume were created. The values of speed of sound (SOS) and broadband ultrasound attenuation (BUA) were calculated through the finite element simulations of ultrasound propagation in each sample. Comparing the results with other experimental and simulation studies demonstrated the capabilities of the FEM for micro-scale modeling of ultrasound in water-saturated cancellous bone.     

Investigation of an anisotropic tortuosity in a biot model of ultrasonic propagation in cancellous bone

The modeling of ultrasonic propagation in cancellous bone is relevant to the study of clinical bone assessment. Historical experiments revealed the importance of both the viscous effects of bone marrow and the anisotropy of the porous microstructure. Of those propagation models previously applied to cancellous bone, Biot's theory incorporates viscosity, but has only been applied in isotropic form, while Schoenberg's anisotropic model does not include viscosity. In this paper we present an approach that incorporates the merits of both models, by utilizing the tortuosity, a key parameter describing pore architecture. An angle-dependent tortuosity for a layered structure is used in Biot's theory to generate the "Stratified Biot Model" for cancellous bone, which is compared with published bone data. While the Stratified Biot model was inferior to Schoenberg's model for slow wave velocity prediction, the proposed model improved agreement fast wave velocity at high propagation angles, particularly when sorted for porosity. An attempt was made to improve the fast wave agreement at low angles by introducing an angle-dependent Young's Modulus, which, while improving the agreement of predicted fast wave velocity at low angles, degraded agreement at high angles. In this paper the utility of the tortuosity in characterizing the architecture of cancellous bone is highlighted.     

Estimation of critical and viscous frequencies for Biot theory in cancellous bone

The use of Biot theory for modelling ultrasonic wave propagation in porous media involves the definition of a "critical frequency" above which both fast and slow compressional waves will, in principle, propagate. Critical frequencies have been evaluated for healthy and osteoporotic cancellous bone filled with water or marrow, using data from the literature. The range of pore sizes in bone gives rise to a critical frequency band rather than a single critical frequency, the mean of which is lower for osteoporotic bone than normal bone. However, the critical frequency is a theoretical concept and previous researchers considered a more realistic "viscous frequency" above which both fast and slow waves may be experimentally observed. Viscous frequencies in bone are found to be several orders of magnitude greater than calculated critical frequencies. Whereas two waves may well be observed at all ultrasonic frequencies for water-filled cancellous bone at 20 degrees C, it is probable megahertz frequencies would be needed for observation of two waves in vivo.     

Phase and group velocities of fast and slow compressional waves in trabecular bone

This Letter is an extension to a multilayer model of porous bone first proposed by Hughes et al. [Ultrasound Med. Biol. 25, 811-821 (1999)]. Both slow and fast compressional waves propagate when the acoustic wave propagation is parallel to the trabecular alignment. However, a slow wave disappears at high refraction angles. To explain this phenomenon, the multilayer model is extended to compute group velocity surface and arrival times with an angle. Two major effects are highlighted as the refraction angle increases. First, the energy of the slow wave is refracted from the phase propagation direction. Second, the signals of fast and slow waves overlap. As a consequence, the slow wave may not be observed for a refraction angle greater than 40 degrees, which is in agreement with previous experimental data published by Hughes et al. and others.     

Cancellous bone analysis with modified least squares Prony's method and chirp filter: phantom experiments and simulation

The presence of two longitudinal waves in porous media is predicted by Biot's theory and has been confirmed experimentally in cancellous bone. When cancellous bone samples are interrogated in through-transmission, these two waves can overlap in time. Previously, the Modified Least-Squares Prony's (MLSP) method was validated for estimation of amplitudes, attenuation coefficients, and phase velocities of fast and slow waves, but tended to overestimate phase velocities by up to about 5%. In the present paper, a pre-processing chirp filter to mitigate the phase velocity bias is derived. The MLSP/chirp filter (MLSPCF) method was tested for decomposition of a 500 kHz-center-frequency signal containing two overlapping components: one passing through a low-density-polyethylene plate (fast wave) and another passing through a cancellous-bone-mimicking phantom material (slow wave). The chirp filter reduced phase velocity bias from 100 m/s (5.1%) to 69 m/s (3.5%) (fast wave) and from 29 m/s (1.9%) to 10 m/s (0.7%) (slow wave). Similar improvements were found for 1) measurements in polycarbonate (fast wave) and a cancellous-bone-mimicking phantom (slow wave), and 2) a simulation based on parameters mimicking bovine cancellous bone. The MLSPCF method did not offer consistent improvement in estimates of attenuation coefficient or amplitude.     

Fast wave ultrasonic propagation in trabecular bone: numerical study of the influence of porosity and structural anisotropy

Our goal is to assess the potential of computational methods as an alternative to analytical models to predict the two longitudinal wave modes observed in cancellous bone and predicted by the Biot theory. A three-dimensional (3D) finite-difference time-domain method is coupled with 34 human femoral trabecular microstructures measured using microcomputed tomography. The main trabecular alignment (MTA) and the degree of anisotropy (DA) were assessed for all samples. DA values were comprised between 1.02 and 1.9. The influence of bone volume fraction (BV/TV) between 5% and 25% on the properties of the fast and slow waves was studied using a dedicated image processing algorithm to modify the initial 3D microstructures. A heuristic method was devised to determine when both wave modes are time separated. The simulations (performed in three perpendicular directions) predicted that both waves generally overlap in time for a direction of propagation perpendicular to the MTA. When these directions are parallel, both waves are separated in time for samples with high DA and BV/TV values. A relationship was found between the least bone volume fraction required for the observation of nonoverlapping waves and the degree of anisotropy: The higher the DA, the lower the least BV/TV.     

Measurements of ultrasound velocity and attenuation in numerical anisotropic porous media compared to Biot’s and multiple scattering models

This article quantitatively investigates ultrasound propagation in numerical anisotropic porous media with finite-difference simulations in 3D. The propagation media consist of clusters of ellipsoidal scatterers randomly distributed in water, mimicking the anisotropic structure of cancellous bone. Velocities and attenuation coefficients of the ensemble-averaged transmitted wave (also known as the coherent wave) are measured in various configurations. As in real cancellous bone, one or two longitudinal modes emerge, depending on the micro-structure. The results are confronted with two standard theoretical approaches: Biot’s theory, usually invoked in porous media, and the Independent Scattering Approximation (ISA), a classical first-order approach of multiple scattering theory. On the one hand, when only one longitudinal wave is observed, it is found that at porosities higher than 90% the ISA successfully predicts the attenuation coefficient (unlike Biot’s theory), as well as the existence of negative dispersion. On the other hand, the ISA is not well suited to study two-wave propagation, unlike Biot’s model, at least as far as wave speeds are concerned. No free fitting parameters were used for the application of Biot’s theory. Finally we investigate the phase-shift between waves in the fluid and the solid structure, and compare them to Biot’s predictions of in-phase and out-of-phase motions.     

Theoretical and experimental study of the ultrasonic attenuation in bovine cancellous bone

In this study a theoretical approach for the estimation of ultrasonic attenuation is proposed. The approach combines two models which take into account both absorption and scattering. Attenuation due to absorption is studied by using the Biot’s analytical model whereas that due to scattering is described by means of a generalized weak scattering model which is formulated for binary mixtures. The scattering model takes account of the density fluctuation of the porous medium in addition to the propagation velocity fluctuation. For the calculation of the attenuation coefficient due to absorption, experimental values have been used to link size of pores to porosity. The theoretical results have been compared with experimental data obtained on bovine cancellous bone samples filled with water. Using an immersion acoustic transmission method, the ultrasonic attenuation has been measured at a frequency range between 0.1 and 1.0 MHz for 12 bovine cancellous bone samples with a porosity range between 40% and 70%. The prediction of attenuation with this model appears to correspond more closely to its experimentally observed behavior. This study indicates that scattering is the predominant mechanism which is responsible for attenuation in trabecular bone. Furthermore, it shows that the density fluctuations contribute significantly to the phenomenon of attenuation and cannot thus be neglected.     

Vertebral cancellous bone turn-over: microcallus and bridges in backscatter electron microscopy

Backscatter electron microscopy (BSE) is a powerful technique for investigating cancellous bone structure. Its main function is to offer information regarding the degree of mineralization of the tissue within individual trabeculae.

To illustrate the qualitative information that can be drawn from BSE imaging technique, we present a study on human vertebral cancellous bone. This tissue is continuously remodeled through osteoclastic resorption and osteoblastic new bone apposition. It is thought that osteoclastic resorption pits are especially deleterious for vertebral bone architecture since they often perforate the thin trabeculae; the osteoblasts being unable to repair the gap. In addition, excessive stress may also disrupt the architecture in case of trabecular fracture or damage accumulation.

Waves of new bone formation were easy to identify in BSE. Often these waves were connecting both edges of a perforation and called bridges. Additionally, we present a few images of microcallus formations. A microcallus is described as a small mass of woven bone that generally repairs a trabecula. The microstructural aspects of different microcalluses are presented and discussed. Both bridges and microcallus should be considered as examples of the repair porcess since they obviously preserve the connectivity of the trabeculae. However, bridges were much more frequent than microcallus (396 vs 15). Both mechanisms probably illustrate the normal response to different local stimuli.     

Application of an effective medium theory for modeling ultrasound wave propagation in healing long bones

Quantitative ultrasound has recently drawn significant interest in the monitoring of the bone healing process. Several research groups have studied ultrasound propagation in healing bones numerically, assuming callus to be a homogeneous and isotropic medium, thus neglecting the multiple scattering phenomena that occur due to the porous nature of callus. In this study, we model ultrasound wave propagation in healing long bones using an iterative effective medium approximation (IEMA), which has been shown to be significantly accurate for highly concentrated elastic mixtures. First, the effectiveness of IEMA in bone characterization is examined: (a) by comparing the theoretical phase velocities with experimental measurements in cancellous bone mimicking phantoms, and (b) by simulating wave propagation in complex healing bone geometries by using IEMA. The original material properties of cortical bone and callus were derived using serial scanning acoustic microscopy (SAM) images from previous animal studies. Guided wave analysis is performed for different healing stages and the results clearly indicate that IEMA predictions could provide supplementary information for bone assessment during the healing process. This methodology could potentially be applied in numerical studies dealing with wave propagation in composite media such as healing or osteoporotic bones in order to reduce the simulation time and simplify the study of complicated geometries with a significant porous nature.