Noninvasive muscle tension measurement using the novel technique of magnetic resonance elastography (MRE)

A novel method for direct measurement of the state of skeletal muscle contraction is introduced called magnetic resonance elastography (MRE). Such a technique is useful for avoiding the indeterminacy inherent in most inverse dynamic models of the musculoskeletal system. Within a standard MRI scanner, mechanical vibration is applied to muscle via the skin, creating shear waves that penetrate the tissue and propagate along muscle fibers. A gradient echo sequence is used with cyclic motion-encoding to image the propagating shear waves using phase contrast. Individual muscles of interest are identified and the shear wavelength in each is measured. Shear wavelength increases with increasing tissue stiffness and increasing tissue tension.

Several ankle muscles were tested simultaneously in normal subjects. Applied ankle moment was isometrically resisted at several different foot positions. Shear wavelengths in relaxed muscle in neutral foot position was 2.34±0.47 cm for tibialis anterior (TA) and 3.13±0.24 cm for lateral gastrocnemius (LG). Wavelength increased in relaxed muscle when stretched (to 3.80±0.28 cm for TA in 45° plantar-flexion and to 3.95±0.43 cm for LG in 20° dorsi-flexion). Wavelength increased more significantly with contraction (to 7.71±0.97 cm in TA for 16 N m dorsi-flexion effort and to 7.90±0.34 cm in LG for 48 Nm plantar-flexion effort).

MRE has been shown to be sensitive to both passive and active tension within skeletal muscle making it a promising, noninvasive tool for biomechanical analysis. Since it is based on MRI technology, any muscle, however deep, can be interrogated using equipment commonly available in most health care facilities.     

Viscoelastic properties of human cerebellum using magnetic resonance elastography

BackgroundThe cerebellum has never been mechanically characterised, despite its physiological importance in the control of motion and the clinical prevalence of cerebellar pathologies. The aim of this study was to measure the linear viscoelastic properties of the cerebellum in human volunteers using Magnetic Resonance Elastography (MRE).MethodsCoronal plane brain 3D MRE data was performed on eight healthy adult volunteers, at 80 Hz, to compare the properties of cerebral and cerebellar tissues. The linear viscoelastic storage (G′) and loss moduli (G″) were estimated from the MRE wave images by solving the wave equation for propagation through an isotropic linear viscoelastic solid. Contributions of the compressional wave were removed via application of the curl-operator.ResultsThe storage modulus for the cerebellum was found to be significantly lower than that for the cerebrum, for both white and grey matter. Cerebrum: white matter (mean±SD) G′=2.41±0.23 kPa, grey matter G′=2.34±0.22 kPa; cerebellum: white matter, G′=1.85±0.18 kPa, grey matter G′=1.77±0.24 kPa; cerebrum vs cerebellum, p<0.001. For the viscous behaviour, there were differences in between regions and also by tissue type, with the white matter being more viscous than grey matter and the cerebrum more viscous than the cerebellum. Cerebrum: white matter G″=1.21±0.21 kPa, grey matter G″=1.11±0.03 kPa; cerebellum: white matter G″=1.1±0.23 kPa, grey matter G″=0.94±0.17 kPa.DiscussionThese data represent the first available data on the viscoelastic properties of cerebellum, which suggest that the cerebellum is less physically stiff than the cerebrum, possibly leading to a different response to mechanical loading. These data will be useful for modelling of the cerebellum for a range of purposes.     

Assessment of in vivo and post-mortem mechanical behavior of brain tissue using magnetic resonance elastography

The knowledge of in vivo brain tissue mechanical properties is essential in several biomedical engineering fields, such as injury biomechanics and neurosurgery simulation. Almost all existing available data have been obtained in vitro by invasive experimental protocols. However, the difference between in vivo and post-mortem mechanical properties remains poorly known, essentially due to the lack of a common method that could measure them both in vivo and ex vivo. In this study, we report the use of magnetic resonance elastography (MRE) for the non-invasive assessment of in vivo brain tissue viscoelastic properties and for the investigation of their evolution after the death. Experiments were performed on seven adult male rats. Shear storage and loss moduli were measured in vivo, just after death and at post-mortem time of approximately 24h. A significant increase in shear storage modulus G(') of approximately 100% was found to occur just after death (p=0.002), whereas no significant difference was found between in vivoG(') and G(') at 24h post-mortem time. No significant difference was found between shear loss modulus G(')in vivo and just after death, whereas a decrease of about 50% was found to occur after 24h (p=0.02). These results illustrate the ability of MRE to investigate some of the critical soft tissue biomechanics-related issues, as it can be used as a non-invasive tool for measuring soft tissue viscoelastic properties.     

Exercise performance and magnetic resonance imaging-determined thigh muscle volume in children

This study examined the relationships between thigh muscle volume (TMV) and aerobic and anaerobic performance in children. A total of 32 children, 16 boys and 16 girls, aged 9.9 (0.3) years completed a treadmill running test to exhaustion for the determination of peak oxygen uptake (peak V˙O₂) and a Wingate Anaerobic Test (WAnT) for the determination of peak power (PP) and mean power (MP). The volume of the right thigh muscle was determined using magnetic resonance imaging. TMV was not significantly different in boys and girls [2.39 (0.29) l vs 2.18 (0.38) l, P > 0.05]. Peak V˙O₂ and MP were significantly higher in boys than girls (P < 0.01) whether expressed in absolute, mass-related or allometrically scaled terms. Absolute PP was not significantly different in boys and girls but mass-related and allometrically scaled values were higher in boys (P < 0.01). TMV was correlated with absolute peak V˙O₂, PP and MP in both sexes (r = 0.52–0.89, P < 0.01). In boys, mass-related PP was correlated with TMV (r =0.53, P < 0.01), and in girls mass-related peak V˙O₂ was correlated with TMV (r = −0.61, P < 0.01). However, in neither sex were allometrically scaled peak V˙O₂, PP or MP correlated with TMV (P > 0.05). There were no significant differences between boys and girls in terms of peak V˙O₂, PP or MP when expressed in a ratio to TMV or allometrically scaled TMV. In conclusion, this study has demonstrated that, when body size is appropriately accounted for using allometric scaling, TMV is unrelated to indices of aerobic and anaerobic power in 10-year-old children. Furthermore, there appear to be no qualitative differences in the muscle function of boys and girls in respect of aerobic and anaerobic function. Accepted: 4 February 1997     

Characterization of muscle belly elastic properties during passive stretching using transient elastography

Passive muscle stretching can be used in vivo to assess the viscoelastic properties of the entire musculo-articular complex, but does not allow the specific determination of the muscle or tendon viscoelasticity. In this respect, the local muscle hardness (LMH) of the gastrocnemius medialis (GM) belly was measured during a passive ankle stretching of 10 subjects using transient elastography. A Biodex isokinetic dynamometer was used to stretch ankle plantar flexors, to measure ankle angle, and the passive torque developed by the ankle joint in resistance to the stretch. Results show that the LMH increased during the stretching protocol, with an averaged ratio between maximal LMH and minimal LMH of 2.62+/-0.46. Furthermore, LMH-passive torque relationships were nicely fitted using a linear model with mean correlation coefficients (R(2)) of 0.828+/-0.099. A good reproducibility was found for the maximal passive torque (ICC=0.976, SEM=2.9Nm, CV=5.5%) and the y-intercept of the LMH-passive torque relationship (ICC=0.893, SEM=105Pa, CV=7.8%). However, the reproducibility was low for the slope of this relationship (ICC=0.631, SEM=10.35m(-2), CV=60.4%). The y-intercept of the LMH-passive torque relationship was not significantly changed after 10min of static stretching. This result confirms the finding of a previous study indicating that changes in passive torque following static stretching could be explained by an acute increase in muscle length without any changes in musculo-articular intrinsic mechanical properties.     

In-vivo determination of 3D muscle architecture of human muscle using free hand ultrasound

Muscle architecture is an important parameter affecting the muscle function. Most of the previous studies on in-vivo muscle architecture have used in 2D ultrasound. The importance of the third dimension has not been much explored due to lack of appropriate methods. DT-MRI has been used to study muscle architecture in 3D, however, due to long scan times of about 15 min DT-MRI has not been suitable to study active muscle contractions. The purpose of this study was to develop and validate methods to determine in-vivo muscle fascicle orientations in 3D using ultrasound. We have used 2D ultrasound and a 3D position tracker system to find the 3D fascicle orientation in 3D space. 2D orientations were obtained by using automated methods developed in our previous studies and we have extended these in the current study to obtain the 3D muscle fascicle orientation in 3D space. The methods were validated using the physical phantom and we found that the mean error in the measurement was less than 0.5° in each of the three co-ordinate planes. These methods can be achieved with short scan times (less than 2 min for the gastrocnemii) and will thus enable future studies to quantify 3D muscle architecture during sub-maximal voluntary contractions.     

Characterization of a hyper-viscoelastic phantom mimicking biological soft tissue using an abdominal pneumatic driver with magnetic resonance elastography (MRE)

The purpose of this study was to create a polymer phantom mimicking the mechanical properties of soft tissues using experimental tests and rheological models. Multifrequency Magnetic Resonance Elastography (MMRE) tests were performed on the present phantom with a pneumatic driver to characterize the viscoelastic (μ, η) properties using Voigt, Maxwell, Zener and Springpot models. To optimize the MMRE protocol, the driver behavior was analyzed with a vibrometer. Moreover, the hyperelastic properties of the phantom were determined using compressive tests and Mooney-Rivlin model. The range of frequency to be used with the round driver was found between 60 Hz and 100 Hz as it exhibits one type of vibration mode for the membrane. MRE analysis revealed an increase in the shear modulus with frequency reflecting the viscoelastic properties of the phantom showing similar characteristic of soft tissues. Rheological results demonstrated that Springpot model better revealed the viscoelastic properties (μ=3.45 kPa, η=6.17 Pas) of the phantom and the Mooney-Rivlin coefficients were C(10)=1.09.10(-2) MPa and C(01)=-8.96.10(-3) MPa corresponding to μ=3.95 kPa. These studies suggest that the phantom, mimicking soft tissue, could be used for preliminary MRE tests to identify the optimal parameters necessary for in vivo investigations. Further developments of the phantom may allow clinicians to more accurately mimic healthy and pathological soft tissues using MRE.     

Estimation of individual muscle force using elastography

Background

Estimation of an individual muscle force still remains one of the main challenges in biomechanics. In this way, the present study aimed: (1) to determine whether an elastography technique called Supersonic Shear Imaging (SSI) could be used to estimate muscle force, (2) to compare this estimation to that one provided by surface electromyography (EMG), and (3) to determine the effect of the pennation of muscle fibers on the accuracy of the estimation.

Methods and Results

Eleven subjects participated in two experimental sessions; one was devoted to the shear elastic modulus measurements and the other was devoted to the EMG recordings. Each session consisted in: (1) two smooth linear torque ramps from 0 to 60% and from 0 to 30% of maximal voluntary contraction, for the first dorsal interosseous and the abductor digiti minimi, respectively (referred to as “ramp contraction”); (2) two contractions done with the instruction to freely change the torque (referred to as “random changes contraction”). Multi-channel surface EMG recordings were obtained from a linear array of eight electrodes and the shear elastic modulus was measured using SSI. For ramp contractions, significant linear relationships were reported between EMG activity level and torque (R² = 0.949±0.036), and between shear elastic modulus and torque (R² = 0.982±0.013). SSI provided significant lower RMS_deviation between measured torque and estimated torque than EMG activity level for both types of contraction (1.4±0.7 vs. 2.8±1.4% of maximal voluntary contraction for “ramp contractions”, p<0.01; 4.5±2.3 vs. 7.9±5.9% of MVC for “random changes contractions”, p<0.05). No significant difference was reported between muscles.

Conclusion

The shear elastic modulus measured using SSI can provide a more accurate estimation of individual muscle force than surface EMG. In addition, pennation of muscle fibers does not influence the accuracy of the estimation.     

Wave attenuation as a measure of muscle quality as measured by magnetic resonance elastography: Initial results

Advances in imaging technologies such as magnetic resonance elastography (MRE) have allowed researchers to gain insights into muscle function in vivo. MRE has been used to examine healthy and diseased muscle by calculating shear modulus. However, additional information can be measured from visualizing a mechanical wave as it passes through a tissue. One such measurable quantity is wave attenuation. The purpose of this study was to determine if a simple measure of wave attenuation could be used to distinguish between healthy and diseased muscle. Twenty seven subjects (14 healthy controls, 7 hyperthyroid myopathy patients, 6 myositis patients) participated in this study. Wave amplitude was determined along a linear profile through the center of the muscle, and an exponential decay curve was fit to the data. This measure was able to find significant differences in attenuation between healthy and diseased muscle. Furthermore, four hyperthyroid myopathy subjects who were tested following treatment all showed improvement by this measure. A likely reason for patients with hyperthyroid myopathy and myositis behaving similarly is that this measurement may reflect similar changes in the muscle extracellular matrix. In addition to modulus, attenuation seems to be an important parameter to measure in skeletal muscle. Further research is needed to investigate other potential measures of attenuation as well as examining other potential measures that can be found from visualizing wave propagation. Future studies should also include muscle biopsies to confirm that the changes seen are as a result of changes in extracellular matrix structure.     

Age-related changes in human skeletal muscle microstructure and architecture assessed by diffusion-tensor magnetic resonance imaging and their association with muscle strength

Diffusion-tensor magnetic resonance imaging (DT-MRI) offers objective measures of muscle characteristics, providing insights into age-related changes. We used DT-MRI to probe skeletal muscle microstructure and architecture in a large healthy-aging cohort, with the aim of characterizing age-related differences and comparing these to muscle strength. We recruited 94 participants (43 female; median age = 56, range = 22–89 years) and measured microstructure parameters—fractional anisotropy (FA) and mean diffusivity (MD)—in 12 thigh muscles, and architecture parameters—pennation angle, fascicle length, fiber curvature, and physiological cross-sectional area (PCSA)—in the rectus femoris (RF) and biceps femoris longus (BFL). Knee extension and flexion torques were also measured for comparison to architecture measures. FA and MD were associated with age (β = 0.33, p = 0.001, R² = 0.10; and β = −0.36, p < 0.001, R² = 0.12), and FA was negatively associated with Type I fiber proportions from the literature (β = −0.70, p = 0.024, and R² = 0.43). Pennation angle, fiber curvature, fascicle length, and PCSA were associated with age in the RF (β = −0.22, 0.26, −0.23, and −0.31, respectively; p < 0.05), while in the BFL only curvature and fascicle length were associated with age (β = 0.36, and −0.40, respectively; p < 0.001). In the RF, pennation angle and PCSA were associated with strength (β = 0.29, and 0.46, respectively; p < 0.01); in the BFL, only PCSA was associated with strength (β = 0.43; p < 0.001). Our results show skeletal muscle architectural changes with aging and intermuscular differences in the microstructure. DT-MRI may prove useful for elucidating muscle changes in the early stages of sarcopenia and monitoring interventions aimed at preventing age-associated microstructural changes in muscle that lead to functional impairment.     

Demonstration of primary and secondary muscle fiber architecture of the bovine tongue by diffusion tensor magnetic resonance imaging

The myoarchitecture of the tongue is comprised of a complex array of muscle fiber bundles, which form the structural basis for lingual deformations during speech and swallowing. We used magnetic resonance imaging of the water diffusion tensor to display the primary and secondary fiber architectural attributes of the excised bovine tongue. Fiber orientation mapping provides a subdivision of the tongue into its principal intrinsic and extrinsic muscular components. The anterior tongue consists of a central region of orthogonally oriented intrinsic fibers surrounded by an axially oriented muscular sheath. The posterior tongue consists principally of a central region of extrinsic fibers, originating at the inferior surface and projecting in a fan-like manner in the superior, lateral, and posterior directions, and lateral populations of extrinsic fibers directed posterior-inferior and posterior-superior. Analysis of cross-fiber anisotropy indicates a basic contrast of design between the extrinsic and the intrinsic fibers. Whereas the extrinsic muscles exhibit a uniaxial architecture typical of skeletal muscle, the intrinsic core muscles, comprised of the verticalis and the transversus muscles, show strong cross-fiber anisotropy. This pattern is consistent with the theory that the tongue's core functions as a muscular hydrostat in that conjoint contraction of the transverse and vertical fibers enable the tissue to expand at right angles to these fibers. These findings suggest that three-dimensional analysis of diffusion tensor magnetic resonance imaging provides a structural basis for understanding the micromechanics of the mammalian tongue.     

Possibilities of using magnetic resonance imaging-transrectal ultrasound fusion in the diagnosis of recurrent prostate cancer

This paper considers whether magnetic resonance imaging (MRI) and transrectal ultrasound (TRUS) can be fused, by applying an external bobbin with transrectal ultrasound imaging. The author has studied whether imaging fusion can be used to select a targeted needle biopsy (NB) portion if the development of recurrent prostate cancer (PC) is suspected after radical prostatectomy (RP). MRI-TRUS fusion was performed in 11 patients in different periods after RP. All the patients underwent dynamic contrast-enhanced MRI and then MRI-TRUS fusion during TRUS studies (TRUSS). MRI-TRUS fusion-guided NBs of suspected portions in the vesicourethral anastomotic area were carried out in 7 patients. A control group comprised 18 patients, of whom 12 patients underwent isolated TRUS-guided NB. The use of the fusion technology was shown to make a simultaneous assessment of the MRI and TRUS images of a vesicourethral anastomotic area in post-RP patients. At the same time, the high accuracy of comparison of MRI and TRUS images ensures the steady position of portions with early intensive accumulation of a MRI contrast agent during real-time TRUSS. Thus, morphologically relevant materials could be obtained in 6 of the 7 patients in the MRI-TRUS-guided NB group and only in 3 of the 12 control patients. Therefore, the use of MRI-TRUS fusion enhances the efficiency of NB in post-RP patients suspected of having recurrent PC. The criterion for selecting a target portion is the abnormal accumulation of a MRI contrast agent.