In vitro ultrasonic characterization of human cancellous femoral bone using transmission and backscatter measurements: relationships to bone mineral density

Thirty-eight slices of pure trabecular bone 1-cm thickness were extracted from human proximal femurs. A pair of 1-MHz central frequency transducers was used to measure quantitative ultrasound (QUS) parameters in transmission [normalized broadband ultrasound attenuation (nBUA), speed of sound (SOS)] and in backscatter [broadband ultrasound backscatter (BUB)]. Bone mineral density (BMD) was measured using clinical x-ray quantitative computed tomography. Site-matched identical region of interest (ROIs) of 7 x 7 mm2 were positioned on QUS and QCT images. This procedure resulted in 605 ROIs for all the specimens data pooled together. The short-term precision of the technique expressed in terms of CV was found to be 2.3% for nBUA, 0.3% for SOS and 4.5% for BUB. Significant linear correlation between QUS and BMD were found for all the 605 ROIs pooled, with r2 values of 0.73, 0.77, and 0.58 for nBUA, SOS, and BUB, respectively (all p < 0.05). For the BUB, the best regression was obtained with a polynomial fit of second order (r2 = 0.63). An analysis of measurements errors was developed. It showed that the residual variability of SOS is almost completely predicted by measurements errors, which is not the case for BUA and BUB, suggesting a role for micro-architecture in the determination of BUA and BUB.     

Relationships among calcaneal backscatter, attenuation, sound speed, hip bone mineral density, and age in normal adult women

The present study was undertaken in order to investigate the use of calcaneal ultrasonic backscatter for the application of diagnosis of osteoporosis. Broadband ultrasonic attenuation (BUA), speed of sound (SOS), the average backscatter coefficient (ABC), and the hip bone mineral density (BMD) were measured in calcanea in 47 women (average age: 58 years, standard deviation: 13 years). All three ultrasound variables had comparable correlations with hip BMD (around 0.5). As reported previously by others, BUA and SOS were rather highly correlated with each other. The logarithm of the ABC was only moderately correlated with the other two. The three ultrasound parameters exhibited similar moderate negative correlations with age. These results taken collectively suggest that the ABC may carry important diagnostic information independent of that contained in BUA and SOS and, therefore, may be useful as an adjunct measurement in the diagnosis of osteoporosis.     

An investigation of the measurement of broadband ultrasonic attenuation in trabecular bone

Commercial devices for the ultrasonic characterisation of bone normally report the broadband ultrasonic attenuation (BUA). This is the slope of the attenuation against frequency in some part of the frequency range 200–1000 kHz. The assumption is that the relationship is linear and hence independent of the frequency range selected. In this study the ultrasonic attenuation in the frequency range 200 to 800 kHz was measured with a variety of transducers in ten trabecular heel bone samples from elderly cadavers, assumed to be osteoporotic.

The results indicate that the attenuation fits better to a second order polynomial function of frequency, than to the linear fit. The use of a straight line fit is only satisfactory in the higher frequency ranges (above 400 kHz). The use of lower frequencies results in a significant measurement error caused by the combination of a poor signal to noise ratio and the departure from linearity and this is greatest for samples with low attenuation. In the worst cases this can amount to a 30% discrepancy between the BUA values measured over different frequency ranges.     

Influence of microarchitecture alterations on ultrasonic backscattering in an experimental simulation of bovine cancellous bone aging

An experimental model which can simulate physical changes that occur during aging was developed in order to evaluate the effects of change of mineral content and microstructure on ultrasonic properties of bovine cancellous bone. Timed immersion in hydrochloric acid was used to selectively alter the mineral content. Scanning electron microscopy and histological staining of the acid-treated trabeculae demonstrated a heterogeneous structure consisting of a mineralized core and a demineralized layer. The presence of organic matrix contributed very little to normalized broadband ultrasound attenuation (nBUA) and speed of sound. All three ultrasonic parameters, speed of sound, nBUA and backscatter coefficient, were sensitive to changes in apparent density of bovine cancellous bone. A two-component model utilizing a combination of two autocorrelation functions (a densely populated model and a spherical distribution) was used to approximate the backscatter coefficient. The predicted attenuation due to scattering constituted a significant part of the measured total attenuation (due to both scattering and absorption mechanisms) for bovine cancellous bone. Linear regression, performed between trabecular thickness values and estimated from the model correlation lengths, showed significant linear correlation, with R(2)=0.81 before and R(2)=0.80 after demineralization. The accuracy of estimation was found to increase with trabecular thickness.     

Detection of bone disease with ultrasound--comparison with bone densitometry

A system for ultrasonic in-vivo examination of a heel bone (calcaneus) was developed. When operating in transmission mode, the system can measure broadband ultrasonic attenuation-BUA, speed of sound--SOS and thickness of bone. BUA and SOS are measured by comparing the pulses transmitted through the heel with the reference pulse transmitted through water. In our approach, we operate in the backscattered mode in addition to transmission. The backscattered ultrasonic technique for bone characterization is very promising because the magnitude of backscattered waves depends on the scattering cross-section of a trabecular structure that, to some extent, describes the microarchitecture of a calcaneus. Additionally, when the backscattered and transmitted signals are compared, some of the signal distortions caused by tissue and bone interfaces are reduced. A set of data representing signals transmitted through the heel and reflected inside a calcaneus for patients with osteoporosis was collected. Several signal-processing techniques were applied in order to smooth the backscattered signal and to calculate a trabecular structure cros-section (TSC) function. Results obtained by these approaches along with a spectral shift method and a standard BUA measurement are presented and compared to X-ray bone mineral density determination results.     

Characterization of dense bovine cancellous bone tissue microstructure by ultrasonic backscattering using weak scattering models

A weak scattering model was proposed for the ultrasonic frequency-dependent backscatter in dense bovine cancellous bone, using two autocorrelation functions to describe the medium: one with discrete homogeneities (spherical distribution of equal spheres) and another, which considers tissue as an inhomogeneous continuum (densely populated medium). The inverse problem to estimate trabecular thickness of bone tissue has been addressed. A combination of the two autocorrelation functions was required to closely approximate the backscatter from bovine bone with various microarchitecture, given that the shape of trabeculae ranges from a rodlike to a platelike shape. Because of the large variation in trabecular thickness, both at an intraspecimen and an interspecimen level, thickness distributions for individual trabeculae for each bone specimen were obtained, and dominant trabecular sizes were determined. Comparison of backscatter measurements to theoretical predictions indicated that there were more than one dominant trabecular sizes that scatter sound for most specimens. Linear regression, performed between dominant trabecular thickness and estimated correlation length, showed significant linear correlation (R(2)=0.81). Attenuation due to scattering by a continuous distribution of scatterers was predicted to be linear over a frequency range from 0.3 to 0.9 MHz, suggesting a possibility that scattering may be a significant source of attenuation.     

Estimation of ultrasonic attenuation in a bone using coded excitation

This paper describes a novel approach to estimate broadband ultrasound attenuation (BUA) in a bone structure in human in vivo using coded excitation. BUA is an accepted indicator for assessment of osteoporosis. In the tested approach a coded acoustic signal is emitted and then the received echoes are compressed into brief, high amplitude pulses making use of matched filters and correlation receivers. In this way the acoustic peak pressure amplitude probing the tissue can be markedly decreased whereas the average transmitted intensity increases proportionally to the length of the code. This paper examines the properties of three different transmission schemes, based on Barker code, chirp and Golay code. The system designed is capable of generating 16 bits complementary Golay code (CGC), linear frequency modulated (LFM) chirp and 13-bit Barker code (BC) at 0.5 and 1 MHz center frequencies. Both in vivo data acquired from healthy heel bones and in vitro data obtained from human calcaneus were examined and the comparison between the results using coded excitation and two cycles sine burst is presented. It is shown that CGC system allows the effective range of frequencies employed in the measurement of broadband acoustic energy attenuation in the trabecular bone to be doubled in comparison to the standard 0.5 MHz pulse transmission. The algorithm used to calculate the pairs of Golay sequences of the different length, which provide the temporal side-lobe cancellation is also presented. Current efforts are focused on adapting the system developed for operation in pulse-echo mode; this would allow examination and diagnosis of bones with limited access such as hip bone.     

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.     

Relationships between the anisotropy of longitudinal wave velocity and hydroxyapatite crystallite orientation in bovine cortical bone

Quantitative ultrasound (QUS) is now widely used for evaluating bone in vivo, because obtained ultrasonic wave properties directly reflect the visco-elasticity. Bone tissue is composed of minerals like hydroxyapatite (HAp) and a collagen matrix. HAp crystallites orientation is thus one parameter of bone elasticity. In this study, we experimentally investigated the anisotropy of ultrasonic wave velocity and the HAp crystallites orientation in the axial-radial and axial-tangential planes in detail, using cylindrical specimens obtained from the cortical bone of three bovine femurs. Longitudinal bulk wave propagation was investigated by using a conventional ultrasonic pulse system. We used the one cycle of sinusoidal pulse which was emitted from wide band transmitter. The nominal frequency of the pulse was 1 MHz. First, we investigated the anisotropy of longitudinal wave velocity, measuring the anisotropy of velocity in two planes using cylindrical specimens obtained from identical bone areas. The wave velocity changed due to the rotation angle, showing the maximum value in the direction a little off the bone axis. Moreover, X-ray pole figure measurements also indicated that there were small tilts in the HAp crystallites orientation from the bone axis. The tilt angles were similar to those of the highest velocity direction. There were good correlations between velocity and HAp crystallites orientation obtained in different directions. However, a comparatively low correlation was found in posterior bone areas, which shows the stronger effects of bone microstructure. In the radial-tangential plane, where the HAp crystallites hardly ever align, weak anisotropy of velocity was found which seemed to depend on the bone microstructure.     

Distribution of longitudinal wave properties in bovine cortical bone in vitro

The detailed spatial distributions of longitudinal ultrasonic velocity in cortical bone specimens obtained from three bovine femoral diaphysis were experimentally investigated using a pulse-echo system. The relationship between velocity, density, bone mineral density (BMD) and microstructure was investigated. Velocity was found to vary as a function of the direction of propagation and the location of the measured specimens in the bone diaphysis. A significant correlation was found between density and velocity, and between density and BMD. In some parts with plexiform structure, clear variations in velocity anisotropy were found despite no significant difference in density, BMD and microstructure.     

Control of acoustic beam angle by harmonic analysis of sequential samples from a multi-element linear array

Frequency components contained within the sequential samples of a linear array of ultrasonic receiver transducers are shown to be a function of the angle of incidence of the received energy. The principle has been successfully confirmed by experimental results which provide both the range and bearing of multiple targets. The equipment used was operated at an ultrasonic frequency of 500 kHz and the array sampled at rates of 2.26 and 4.52 MHz. Finally, a system is proposed where the target information is given on a sector PPI display.     

Frequency dependence of ultrasonic backscatter from human trabecular bone: theory and experiment

A model describing the frequency dependence of backscatter coefficient from trabecular bone is presented. Scattering is assumed to originate from the surfaces of trabeculae, which are modeled as long thin cylinders with radii small compared with the ultrasonic wavelength. Experimental ultrasonic measurements at 500 kHz, 1 MHz, and 2.25 MHz from a wire target and from trabecular bone samples from human calcaneus in vitro are reported. In both cases, measurements are in good agreement with theory. For mediolateral insonification of calcaneus at low frequencies, including the typical diagnostic range (near 500 kHz), backscatter coefficient is proportional to frequency cubed. At higher frequencies, the frequency response flattens out. The data also suggest that at diagnostic frequencies, multiple scattering effects on the average are relatively small for the samples investigated. Finally, at diagnostic frequencies, the data suggest that absorption is likely to be a larger component of attenuation than scattering.     

Correlations of group velocity, phase velocity, and dispersion with bone density in bovine trabecular bone

The present study investigated the correlations of the group velocity, the phase velocity, and the velocity dispersion with the apparent bone density in bovine trabecular bone in vitro. The phase velocity exhibited the negative dispersion, consistent with the behavior in human trabecular bone. The group and the phase velocities were found to increase with increasing apparent bone density, respectively, exhibiting similar high correlations of r=0.94 and 0.96. The negative dispersion rate exhibited a decreasing dependence on the apparent bone density, with a significant correlation of r=-0.86.     

Study for imaging of inside bone using FM-chirp pulse compression system

We measured the attenuation of ultrasound in animal bone in vitro, and determined successfully the correct dynamic range for the detection of echo signals from inside the bone. It was possible to display a B-mode image of a 6-mm thick porcine rib bone using a high frequency (5 MHz) transducer. However, it was difficult to obtain the image of a large bone (20-mm thick femur). This paper describes a possibility of the improvement for the detection of echoes from inside the bone using the FM-chirp pulse. An ultrasonic wave generator that generates the FM-chirp pulse for a frequency range of 100 KHz to 5 MHz was fabricated. And the pulse was transmitted from a transducer and received by a hydrophone in the water. The received waveform and the frequency spectrum were displayed on an oscilloscope. We measured the amplitude spectrum of the received waves before and after inserting a sample bone between the transducer and the hydrophone. In the experiment, three types of focused transducers (0.5, 1 and 2.25 MHz) and three kinds of sample bones (spine, femur and rib of a pig) were used. From the results of the measurement, we could find the useful information for imaging of inside the bone.     

面向水下应用的电容式微机械超声换能器*

电容式微机械超声换能器具有宽频带和易于制造二维阵列等优势,已经成为一种重要的新型超声换能器。该文针对图像声呐系统对新型超声换能器的迫切需求,提出了一种电容式微机械超声换能器结构和参数,并利用硅微加工技术制备出了该换能器,最后对其主要性能参数进行了测试和分析。测试结果表明该换能器具有发射和接收超声波的功能,中心工作频率为1.965 MHz,6 dB相对带宽达到109.4%,在1 MHz、2 MHz和3 MHz频率时的接收灵敏度分别为-218.29 d B、-219.39 dB和-218.11 dB。该文研制的电容式微机械超声换能器显示出了优秀的宽频带特性,且工作频率和接收灵敏度性能均基本满足了高频图像声呐系统的需求。     

Feasibility of bone assessment with leaky Lamb waves in bone phantoms and a bovine tibia

In this study, the effect of cortical thickness variation on the propagation of leaky Lamb waves is investigated by using an axial transmission technique commonly used to characterize long bones. Three Lucite plates with thicknesses of 1, 3, and 5 mm as bone phantoms and one bovine tibia with a cortical thickness of 2 mm were used at various low frequencies. Experimental measurements in bone phantoms show that the peak frequency and amplitude of excited Lamb modes strongly depend on the thickness of the Lucite plate. In the bovine tibia, the S0 and A0 Lamb modes are consistently observed in the frequency-thickness region from 0.2 to 1.0 MHz mm, and can be effectively launched at a frequency of 200 kHz, suggesting 200 kHz to be the optimal signal frequency for in vivo clinical applications. It can be also seen that both modes are affected by the frequency-thickness product, but the effect is greater for the A0 mode. Hence, the A0 Lamb mode seems more sensitive to cortical thickness change due to aging and osteoporosis. This study suggests that the use of leaky Lamb waves is feasible for ultrasonic bone assessment.     

Frequency-dependent attenuation and backscatter coefficients in bovine trabecular bone from 0.2 to 1.2 MHz

The frequency-dependent attenuation and backscatter coefficients were measured in 25 bovine femoral trabecular bone samples from 0.2 to 1.2 MHz. When the average attenuation coefficient was fitted to a nonlinear power law α(f)=α(0)+α(1)f(n), the exponent n was found to be 1.65. In contrast, the average backscatter coefficient was fitted to a power law η(f)=η(1)f(n) and the exponent n was measured as 3.25. The apparent bone density was significantly correlated with the parameter α(1) (0.2-0.7 MHz: r = 0.852, 0.6-1.2 MHz: r = 0.832) as well as the backscatter coefficient (0.5 MHz: r = 0.751, 1.0 MHz: r = 0.808).     

空间频率域超声背散射参量用于骨质状况的评价*

在超声背散射骨质评价中,不同测量感兴趣区域(ROI)的超声背散射信号会有波动,致使诊断准确度降低。该文目的是研究超声背散射信号随测量区域的变化规律。采用空间扫描方法离体测量了35块骨样本,将超声背散射参数从空间域变换到空间频率域。结果表明,超声背散射参数的主要空间频率成分集中于低频部分;空间频率域超声背散射参量最大值(MASF)与骨矿密度等参数具有中高度显著相关性(R2=0.45~0.83,p0.001);空间频率域超声背散射参量衰减系数(AC)也与松质骨密度及结构特征有显著相关性(R2=0.41~0.72,p0.001)。研究表明空间频率域变换方法有助于明确超声背散射信号随测量ROI的变化规律,空间频率域的超声背散射相关新参量评价松质骨状况具有可行性。     

Amplitude modulation excitation for cancellous bone evaluation using a portable ultrasonic backscatter instrumentation

The ultrasonic backscatter (UB) has the advantage of non-invasively obtaining bone density and structure, expected to be an assessment tool for early diagnosis osteoporosis. All former UB measurements were based on exciting a short single-pulse and analyzing the ultrasonic signals backscattered in bone. This study aims to examine amplitude modulation (AM) ultrasonic excitation with UB measurements for predicting bone characteristics. The AM multiple lengths excitation and backscatter measurement (AM-UB) functions were integrated into a portable ultrasonic instrument for bone characterization. The apparent integrated backscatter coefficient in the AM excitation (AIB_AM) was evaluated on the AM-UB instrumentation. The correlation coefficients of the AIB_AM estimating volume fraction (BV/TV), structure model index (SMI), and bone mineral density (BMD) were then analyzed. Significant correlations (|R| = 0.82-0.93, p < 0.05) were observed between the AIB_AM, BV/TV, SMI, and BMD. By growing the AM excitation length, the AIB_AM values exhibit more stability both in 1.0-MHz and 3.5-MHz measurements. The recommendations in AM-UB measurement were that the avoided length (T1) should be lower than AM excitation length, and the analysis length (T2) should be enough long but not more than AM excitation length. The authors conducted an AM-UB measurement for cancellous bone characterization. Increasing the AM excitation length could substantially enhance AIB_AM values stability with varying analyzed signals. The study suggests the portable AM-UB instrument with the integration of real-time analytics software that might provide a potential tool for osteoporosis early screening.