Changes in shear wave propagation within skeletal muscle during active and passive force generation

Muscle force can be generated actively through changes in neural excitation, and passively through externally imposed changes in muscle length. Disease and injury can disrupt force generation, but it can be challenging to separate passive from active contributions to these changes. Ultrasound elastography is a promising tool for characterizing the mechanical properties of muscles and the forces that they generate. Most prior work using ultrasound elastography in muscle has focused on the group velocity of shear waves, which increases with increasing muscle force. Few studies have quantified the phase velocity, which depends on the viscoelastic properties of muscle. Since passive and active forces within muscle involve different structures for force transmission, we hypothesized that measures of phase velocity could detect changes in shear wave propagation during active and passive conditions that cannot be detected when considering only group velocity. We measured phase and group velocity in the human biceps brachii during active and passive force generation and quantified the differences in estimates of shear elasticity obtained from each of these measurements. We found that measures of group velocity consistently overestimate the shear elasticity of muscle. We used a Voigt model to characterize the phase velocity and found that the estimated time constant for the Voigt model provided a way to distinguish between passive and active force generation. Our results demonstrate that shear wave elastography can be used to distinguish between passive and active force generation when it is used to characterize the phase velocity of shear waves propagating in muscle.     

Quantifying extensibility of rotator cuff muscle with tendon rupture using shear wave elastography: A cadaveric study

Surgical repair for large rotator cuff tear remains challenging due to tear size, altered muscle mechanical properties, and poor musculotendinous extensibility. Insufficient extensibility might lead to an incomplete reconstruction; moreover, excessive stresses after repair may result in repair failure without healing. Therefore, estimates of extensibility of cuff muscles can help in pre-surgical planning to prevent unexpected scenarios during surgery. The purpose of this study was to determine if quantified mechanical properties of the supraspinatus muscle using shear wave elastography (SWE) could be used to predict the extensibility of the musculotendinous unit on cadaveric specimens. Forty-five fresh-frozen cadaveric shoulders (25 intact and 20 with rotator cuff tear) were used for the study. Passive stiffness of 4 anatomical regions in the supraspinatus muscle was first measured using SWE. After detaching the distal edge of supraspinatus muscle from other cuff muscles, the detached muscle was axially pulled with the scapula fixed. The correlation between the SWE modulus and the extensibility of the muscle under 30 and 60 N loads was assessed. There was a significant negative correlation between SWE measurements and the experimental extensibility. SWE modulus for the anterior-deep region in the supraspinatus muscle showed the strongest correlation with extensibility under 30 N (r = 0.70, P < 0.001) and 60 N (r = 0.68, P < 0.001). Quantitative SWE assessment for the supraspinatus muscle was highly correlated with extensibility of musculotendinous unit on cadaveric shoulders. This technique may be used to predict the extensibility for rotator cuff tears for pre-surgical planning.     

Spatial-dependent mechanical properties of the heel pad by shear wave elastography

The heel pad plays an important role in gait, and its biomechanical behavior and functionality are determined by its specialized architecture and mechanical properties. The purpose of this study was to apply supersonic shear wave elastography, an ultrasound-based noninvasive modality that can quantitatively estimate the shear stiffness of the tissue, to investigate the spatial-dependent mechanical properties of the heel pad. Measurements were conducted in 40 heel pads of 20 normal participants aged between 20 and 30 years by shear wave elastography. The continuous change in local shear stiffness of the heel pad along the depth direction of the heel pad was measured. The result showed that the mechanical properties of the heel pad were highly heterogeneous but followed a simple and specific pattern that local heel pad shear stiffness was highest beneath the plantar skin and decreased continuously with increasing depth. This finding provides a better understanding of the heel pad biomechanics and basis for further investigation of the heterogeneous properties of the heel pad.     

Spatial variations in Achilles tendon shear wave speed

Supersonic shear imaging (SSI) is an ultrasound imaging modality that can provide insight into tissue mechanics by measuring shear wave propagation speed, a property that depends on tissue elasticity. SSI has previously been used to characterize the increase in Achilles tendon shear wave speed that occurs with loading, an effect attributable to the strain-stiffening behavior of the tissue. However, little is known about how shear wave speed varies spatially, which is important, given the anatomical variation that occurs between the calcaneus insertion and the gastrocnemius musculotendon junction. The purpose of this study was to investigate spatial variations in shear wave speed along medial and lateral paths of the Achilles tendon for three different ankle postures: resting ankle angle (R, i.e. neutral), plantarflexed (P; R – 15°), and dorsiflexed (D; R+15°). We observed significant spatial and posture variations in tendon shear wave speed in ten healthy young adults. Shear wave speeds in the Achilles free tendon averaged 12±1.2 m/s in a resting position, but decreased to 7.2±1.8 m/s with passive plantarflexion. Distal tendon shear wave speeds often reached the maximum tracking limit (16.3 m/s) of the system when the ankle was in the passively dorsiflexed posture (+15° from R). At a fixed posture, shear wave speeds decreased significantly from the free tendon to the gastrocnemius musculotendon junction, with slightly higher speeds measured on the medial side than on the lateral side. Shear wave speeds were only weakly correlated with the thickness and depth of the tendon, suggesting that the distal-to-proximal variations may reflect greater compliance in the aponeurosis relative to the free tendon. The results highlight the importance of considering both limb posture and transducer positioning when using SSI for biomechanical and clinical assessments of the Achilles tendon.     

Shear wave elastography of the supraspinatus muscle and tendon: Repeatability and preliminary findings

Shear wave elastography (SWE) is a promising tool for estimating musculoskeletal tissue properties, but few studies have rigorously assessed its repeatability and sources of error. The objectives of this study were to assess: (1) the extent to which probe positioning error and human user error influence measurement accuracy, (2) intra-user, inter-user, and day-to-day repeatability, and (3) the extent to which active and passive conditions affect shear wave speed (SWS) repeatability. Probe positioning and human usage errors were assessed by acquiring SWE images from custom ultrasound phantoms. Intra- and inter-user repeatability were assessed by two users acquiring five trials of supraspinatus muscle and tendon SWE images from ten human subjects. To assess day-to-day repeatability, five of the subjects were tested a second time, approximately 24 h later. Imaging of the phantoms indicated high inter-user repeatability, with intraclass correlation coefficient (ICC) values of 0.68–0.85, and RMS errors of no more than 4.1%. SWE imaging of the supraspinatus muscle and tendon had high repeatability, with intra- and inter-user ICC values of greater than 0.87 and 0.73, respectively. Day-to-day repeatability demonstrated ICC values greater than 0.33 for passive muscle, 0.48 for passive tendon, 0.65 for active muscle, and 0.94 for active tendon. This study indicates the technique has good to very good intra- and inter-user repeatability, and day-to-day repeatability is appreciably higher when SWE images are acquired under a low level of muscle activation. The findings from this study establish the feasibility and repeatability of SWE for acquiring data longitudinally in human subjects.     

Analyzing acoustoelastic effect of shear wave elastography data for perfused and hydrated soft tissues using a macromolecular network inspired model

Shear wave elastography (SWE) has enhanced our ability to non-invasively make in vivo measurements of tissue elastic properties of animal and human tissues. Recently, researchers have taken advantages of acoustoelasticity in SWE to extract nonlinear elastic properties from soft biological tissues. However, most investigations of the acoustoelastic effects of SWE data (AE-SWE) rely on classic hyperelastic models for rubber-like (dry) materials. In this paper, we focus solely on understanding acoustoelasticity in soft hydrated tissues using SWE data and propose a straightforward approach to modeling the constitutive behavior of soft tissue that has a direct microstructural/macromolecular interpretation. Our approach incorporates two constitutive features relevant to biological tissues into AE-SWE: static dilation of the medium associated with nonstructural components (e.g. tissue hydration and perfusion) and finite extensibility derived from an ideal network of biological filaments. We evaluated the proposed method using data from an in-house tissue-mimicking phantom experiment, and ex vivo and in vivo AE-SWE data available in the SWE literature. In conclusion, predictions made by our approach agreed well with measurements obtained from phantom, ex vivo and in vivo tissue experiments.     

Quantifying differences in the material properties of the fiber regions of the pectoralis major using ultrasound shear wave elastography

The sternocostal and clavicular regions of the pectoralis major are independently harvested to provide shoulder stability, but surgical decision making does not consider the biomechanical consequences that disinsertion of one fiber region over the other has on shoulder function. Differences in material properties between the fiber regions could influence which tissue is more optimal for surgical harvesting. The current study utilized ultrasound shear wave elastography (SWE) to investigate whether the in vivo material properties differ between the fiber regions. Shear wave velocities (SWVs) were collected from the sternocostal and clavicular fiber regions of the pectoralis major from ten healthy young male participants. Participants produced isometric shoulder torques of varying magnitudes (passive, 15%, and 30% MVC) and directions (horizontal and vertical adduction). Four shoulder positions encompassing different vertical abduction and external rotation angles were examined. One-way ANOVAs tested the hypotheses that differences in SWVs during rest existed between the fiber regions as a function of shoulder position, and differences in SWVs during contraction existed as a function of shoulder position and torque direction. In all shoulder positions, the clavicular region exhibited greater SWVs during rest than the sternocostal region (P < 0.001). In shoulder positions that did not include external rotation, the clavicular region exhibited greater SWVs during contraction when producing horizontal adduction torques (P < 0.001), while the sternocostal region exhibited greater SWVs during contraction when producing vertical adduction torques at 30% MVC (P < 0.01). Our results suggest that each fiber region of the pectoralis major provides unique contributions to passive and active shoulder function.     

The shear wave elastic modulus and the increased nuclear factor kappa B (NF-kB/p65) and cyclooxygenase-2 (COX-2) expression in the area of myofascial trigger points activated in a rat model by blunt trauma to the vastus medialis

We aimed to elucidate the increased inflammatory cytokines expression such as nuclear factor kappa B (NF-kB/p65), cyclooxygenase-2 (COX-2), and voltage-gated calcium channels (VGCC) in the area of activated myofascial trigger points (MTrPs) in a rat model by blunt trauma to the vastus medialis and to evaluate the feasibility of a quantitative analysis of muscle elastic modulus using shear wave elastography (SWE). Twelve 7-week-old male SD rats were divided into normal (NM, n = 6) and model groups (MO, n = 6). In the MO group, MTrPs were activated with a blunt strike to the left vastus medialis and subsequent eccentric exercise for 8 weeks. After 4 weeks of rest, the elastic modulus in the focal site was evaluated using SWE. Electromyography (EMG) data were collected at MTrPs and muscle tissues were evaluated for expression of nuclear factor kappa B (NF-kB/p65), cyclooxygenase-2 (COX-2) protein, and voltage-gated calcium channels (VGCC). The number of the palpable taut bands; EMG frequency and amplitude; elastic modulus values; and NFkB/p65, COX-2, and VGCC expression levels were significantly higher for the left focal area in the MO group compared to those for the NM group (p’s < 0.05). These findings suggest that elastic modulus measurement using ultrasound SWE may be effective in evaluating MPS. In addition, increased COX-2, NFkB/p65, and VGCC expression may expand the integrated hypothesis of trigger points.     

An ultrasound elastography method to determine the local stiffness of arteries with guided circumferential waves

Arterial stiffness is highly correlated with the functions of the artery and may serve as an important diagnostic criterion for some cardiovascular diseases. To date, it remains a challenge to quantitatively assess local arterial stiffness in a non-invasive manner. To address this challenge, we investigated the possibility of determining arterial stiffness using the guided circumferential wave (GCW) induced in the arterial wall by a focused acoustic radiation force. The theoretical model for the dispersion analysis of the GCW is presented, and a finite element model has been established to calculate the dispersion curve. Our results show that under described conditions, the dispersion relations of the GCW are basically independent of the curvature of the arterial wall and can be well-described using the Lamb wave (LW) model. Based on this conclusion, an inverse method is proposed to characterize the elastic modulus of artery. Both numerical experiments and phantom experiments had been performed to validate the proposed method. We show that our method can be applied to the cases in which the artery has local stenosis and/or the geometry of the artery cross-section is irregular; therefore, this method holds great potential for clinical use.     

Effective muscle elongation positions for the neck extensor muscles: An ultrasonic shear wave elastography study

This study aimed to clarify the effective stretching positions for neck extensor muscles. Fifteen healthy men were measured shear moduli of the right neck extensor muscles using ultrasound shear wave elastography in following positions: rest (Rest), flexion (Flex), contralateral bending (Bend), flexion + contralateral bending (Flex → Bend), flexion + contralateral bending + contralateral rotation (Flex → Bend → ConRot), and flexion + contralateral bending + ipsilateral rotation (Flex → Bend → IpsRot). The increase in the shear modulus indicated a greater muscle elongation. Regarding the upper trapezius and splenius capitis, the shear moduli at Flex → Bend, Flex → Bend → ConRot, and Flex → Bend → IpsRot were significantly higher than those at Rest. The shear moduli at stretching positions, including contralateral bending, were significantly higher than those at Rest and Flex in the levator scapulae. The results indicated that the stretching position with a combination of flexion and contralateral bending could be effective for elongation of the upper trapezius and splenius capitis. Furthermore, the stretching positions including contralateral bending could be effective for the levator scapulae.     

The relationship between muscle activation and shear elastic modulus of the sternocleidomastoid muscle during 3-D torque production

The sternocleidomastoid (SCM) is a primary neck torque generator, but the relationship between its muscle activation and shear elastic modulus during 3-D torque production is unknown. This study examined variations in neural control and shear elastic modulus of the SCM across various 3-D isometric torques. Our primary hypothesis was that the SCM would display similar preferred directions where muscle activity and shear elastic modulus were maximal during voluntary 3-D isometric torque production. Surface electromyography (EMG) and ultrasound shear wave elastography (SWE) data were collected from the SCM in 20 participants performing 3-D isometric target-matching at two different torque amplitudes. We used spherical statistics to compare the preferred directions calculated from the SWE and EMG data at 40% and 80% torque level during 3-D isometric torque production. We demonstrated a small but significant difference between EMG and SWE preferred directions, with the SWE preferred direction oriented more towards ipsilateral bending and less towards contralateral axial rotation than the preferred direction for the EMG data. We conclude that, although small differences exist, SCM shear elastic modulus is largely driven by activation during 3-D neck torques for healthy individuals.     

The effect of three-dimensional postural change on shear elastic modulus of the iliotibial band

To understand and treat iliotibial band (ITB) syndrome, caused by excessive compression between the ITB and lateral femoral condyle, it is important to identify factors contributing to an increase in ITB stiffness. The purpose of this study was to clarify the factors that contribute to an increase in ITB stiffness by examining the relationship between three-dimensional postural changes and ITB stiffness. Fourteen healthy individuals performed one-leg standing under 7 conditions (including normal one-leg standing as a control condition) in which the pelvic position was changed in three planes. The shear elastic modulus in the ITB was measured using shear-wave elastography, as a measure of ITB stiffness. The three-dimensional joint angles and external joint moments in the hip and knee joints were also measured to confirm the changes in joint angles and external load. Compared to the normal one-leg standing condition, ITB stiffness was significantly increased in the pelvic posterior tilted position (i.e. hip extension), contralateral pelvic dropped position (i.e. hip adduction), and contralateral pelvic posterior rotated position (i.e. hip external rotation). The findings suggest that interventions to reduce hip extension, adduction, and external rotation might be useful if these excessive positional changes are detected in patients with ITB syndrome.     

Muscle material properties in passive and active stroke-impaired muscle

Stroke survivors routinely experience long-term motor and sensory impairments. In parallel with neurological changes, material properties of muscles in the impaired limbs, such as muscle stiffness, may also change progressively. However, these stiffness measures are routinely derived from individual joint stiffness, representing whole muscle groups. Here, we use shear wave (SW) ultrasound elastography to measure SW velocity, as a surrogate measure of stiffness, to quantify material properties in individual muscles. Accordingly, the purpose of this study was to compare muscle material properties of the bicep brachii in stroke survivors and in age-matched control subjects by measuring SW velocity at rest and different voluntary activation levels. Our main findings show that at rest, the SW velocity was on average 41% greater in the paretic muscle compared the contralateral non-paretic muscle. The mean passive SW velocity across all subjects were 2.34 ± 0.41 m/s for the non-paretic side, 3.30 ± 1.20 m/s for the paretic side, and 2.24 ± 0.18 for controls. SW velocity was significantly different in muscles of the paretic and non-paretic side (p < 0.001), but not between muscles of the non-paretic and controls (p = 0.47). As voluntary activation increased, SW velocity increased non-linearly, with an average power fit of r² = 0.83 ± 0.09 for the non-paretic side, r² = 0.61 ± 0.24 for the paretic side, and r² = 0.24 ± 0.15 for the healthy age-matched controls. In active muscle (10, 25, 50, 75, 100% maximum voluntary contraction), there was no significant difference in SW velocity between the non-paretic, paretic, and control muscles.These findings suggest that stroke-impaired muscles have potentially altered muscle material properties, specifically stiffness, and that passive and active stiffness may contribute differently to total muscle stiffness.     

Mechanical properties of porcine brain tissue in vivo and ex vivo estimated by MR elastography

The mechanical properties of brain tissue in vivo determine the response of the brain to rapid skull acceleration. These properties are thus of great interest to the developers of mathematical models of traumatic brain injury (TBI) or neurosurgical simulations. Animal models provide valuable insight that can improve TBI modeling. In this study we compare estimates of mechanical properties of the Yucatan mini-pig brain in vivo and ex vivo using magnetic resonance elastography (MRE) at multiple frequencies. MRE allows estimations of properties in soft tissue, either in vivo or ex vivo, by imaging harmonic shear wave propagation. Most direct measurements of brain mechanical properties have been performed using samples of brain tissue ex vivo. It has been observed that direct estimates of brain mechanical properties depend on the frequency and amplitude of loading, as well as the time post-mortem and condition of the sample. Using MRE in the same animals at overlapping frequencies, we observe that porcine brain tissue in vivo appears stiffer than porcine brain tissue samples ex vivo at frequencies of 100 Hz and 125 Hz, but measurements show closer agreement at lower frequencies.     

Site- and sex-differences in morphological and mechanical properties of the plantar fascia: A supersonic shear imaging study

The purpose of this study was to investigate the site- and sex-differences in the morphological and mechanical properties of the plantar fascia (PF) in humans. The thickness and shear wave velocity (SWV) of PF at five different sites between the medial calcaneal tubercle and the second toe were measured for 40 healthy young participants (20 males and 20 females) using supersonic shear imaging (SSI). The thickness and SWV measurements were highly repeatable (ICC ≥ 0.93). The proximal sites of PF around the calcaneal attachment were significantly thicker and stiffer (higher SWV values) than the middle and distal sites (p < 0.05). In addition, females had significantly thinner PF in proximal and middle sites than males, while being significantly stiffer in regardless of the sites, compared with males (p < 0.05). The results of the present study partly support previous findings on the site- and sex-differences in PF morphology, and further reveal inhomogeneity and sex-specificity of PF stiffness. The present study widely opens the possibility of evaluating PF functions in vivo.     

Cervical and axioscapular muscle stiffness measured with shear wave elastography: A comparison between different levels of work-related neck disability

Assessing muscle mechanical properties in terms of stiffness may provide important insights into mechanisms underlying work-related neck pain. This study compared stiffness of cervical and axioscapular muscles between 92 participants (sonographers) with no (n = 31), mild (n = 43) or moderate/severe (n = 18) neck disability. It was hypothesized that participants with more severe neck pain and disability would present with altered distribution of stiffness in cervical and axioscapular muscles than those with no disability. Using shear wave elastography, the shear modulus (kPa) of five cervical and six axioscapular muscles or muscle segments were measured in a relaxed seated upright or side-lying position. Muscle activity was measured simultaneously using surface electromyography during the elastography measurements and scapular depression was measured using a measurement tape and inclinometer before the elastography measurements to evaluate their potential confounding influences on shear modulus. Increased shear modulus was found in deeper than superficial cervical muscles and more cranial than caudal axioscapular muscles. However, no differences in shear modulus of the cervical or axioscapular muscles were found between sonographers with varying levels of disability. This study suggests no alterations in stiffness of cervical and axioscapular muscles were associated with work-related neck pain and disability.     

Calibration of the shear wave speed-stress relationship in ex vivo tendons

It has recently been shown that shear wave speed in tendons is directly dependent on axial stress. Hence, wave speed could be used to infer tendon load provided that the wave speed-stress relationship can be calibrated and remains robust across loading conditions. The purpose of this study was to investigate the effects of loading rate and fluid immersion on the wave speed-stress relationship in ex vivo tendons, and to assess potential calibration techniques. Tendon wave speed and axial stress were measured in 20 porcine digital flexor tendons during cyclic (0.5, 1.0 and 2.0 Hz) or static axial loading. Squared wave speed was highly correlated to stress (r²_avg = 0.98) and was insensitive to loading rate (p = 0.57). The constant of proportionality is the effective density, which reflects the density of the tendon tissue and additional effective mass added by the adjacent fluid. Effective densities of tendons vibrating in a saline bath averaged 1680 kg/m³ and added mass effects caused wave speeds to be 22% lower on average in a saline bath than in air. The root-mean-square error between predicted and measured stress was 0.67 MPa (6.7% of maximum stress) when using tendon-specific calibration parameters. These errors increased to 1.31 MPa (13.1% of maximum stress) when calibrating based on group-compiled data from ten tendons. These results support the feasibility of calculating absolute tendon stresses from wave speed squared based on linear calibration relationships.     

Identification process based on shear wave propagation within a phantom using finite element modelling and magnetic resonance elastography

Magnetic resonance elastography (MRE), based on shear wave propagation generated by a specific driver, is a non-invasive exam performed in clinical practice to improve the liver diagnosis. The purpose was to develop a finite element (FE) identification method for the mechanical characterisation of phantom mimicking soft tissues investigated with MRE technique. Thus, a 3D FE phantom model, composed of the realistic MRE liver boundary conditions, was developed to simulate the shear wave propagation with the software ABAQUS. The assumptions of homogeneity and elasticity were applied to the FE phantom model. Different ranges of mesh size, density and Poisson's ratio were tested in order to develop the most representative FE phantom model. The simulated wave displacement was visualised with a dynamic implicit analysis. Subsequently, an identification process was performed with a cost function and an optimisation loop provided the optimal elastic properties of the phantom. The present identification process was validated on a phantom model, and the perspective will be to apply this method on abdominal tissues for the set-up of new clinical MRE protocols that could be applied for the follow-up of the effects of treatments.     

实时剪切波弹性定量分析不同睾酮水平大鼠阴茎组织硬度

目的:利用实时剪切波弹性成像(shear wave elastography,SWE)定量分析不同睾酮水平阴茎组织硬度之间的差异。方法:睾酮水平不同SD大鼠两组,低睾酮水平组(1月龄,睾酮水平1.00~1.50 ng/m L,n=10)和高睾酮水平组(13月龄,睾酮水平2.00~2.50ng/m L,n=10)。采用放射免疫法测定各组大鼠血清睾酮水平。选用法国Super Sonic Imagine公司生产的Aixplorer超声诊断仪,启动SWE模式对阴茎进行SWE成像并测量其剪切波硬度(shear wave stiffness,SWS)。分析比较两组大鼠血清睾酮水平之间的差异及SWS之间的差异。结果:所有大鼠血清睾酮水平及阴茎组织SWS的测量均成功完成。低睾酮水平组大鼠血清睾酮水平为(1.30±0.16)ng/m L,高睾酮水平组为(2.29±0.14)ng/m L,两组大鼠血清睾酮水平存在显著差异(P0.01);低睾酮水平组大鼠阴茎组织SWS为(9.86±0.72)k Pa,高睾酮水平组为(7.80±1.43)k Pa,两组大鼠阴茎组织SWS存在显著差异(P0.01)。结论:SWE可以检测出睾酮水平不同导致的阴茎组织硬度的差异,提示SWE可作为一项评价阴茎组织硬度的无创新技术。     

In vivo noninvasive measurement of spatially resolved corneal elasticity in human eyes using Lamb wave optical coherence elastography

Current elastography techniques are limited in application to accurately assess spatially resolved corneal elasticity in vivo for human eyes. The air‐puff optical coherence elastography (OCE) with an eye motion artifacts correction algorithm is developed to distinguish the in vivo cornea vibration from the eye motion and visualize the Lamb wave propagation clearly in healthy subjects. Based on the Lamb wave model, the phase velocity dispersion curve in the high‐frequency is calculated to obtain spatially resolved corneal elasticity accurately with high repeatability. It is found that the corneal elasticity has regional variations and is correlated with intraocular pressure, which suggests that the method has the potential to provide noninvasive measurement of spatially resolved corneal elasticity in clinical practice.