Dynamic measurement of pennation angle of gastrocnemius muscles during contractions based on ultrasound imaging

ABSTRACT: BACKGROUND: Muscle fascicle pennation angle (PA) is an important parameter related to musculoskeletal functions, and ultrasound imaging has been widely used for measuring PA, but manually and frame by frame in most cases. We have earlier reported an automatic method to estimate aponeurosis orientation based on Gabor transform and Revoting Hough Transform (RVHT). METHODS: In this paper, we proposed a method to estimate the overall orientation of muscle fascicles in a region of interest, in order to complete computing the orientation of the other side of the pennation angle, but the side found by RVHT. The measurements for orientations of both fascicles and aponeurosis were conducted in each frame of ultrasound images, and then the dynamic change of pennation angle during muscle contraction was obtained automatically. The method for fascicle orientation estimation was evaluated using synthetic images with different noise levels and later on 500 ultrasound images of human gastrocnemius muscles during isometric plantarflexion. RESULTS: The muscle fascicle orientations were also estimated manually by two operators. From the results it's found that the proposed automatic method demonstrated a comparable performance to the manual method. CONCLUSIONS: With the proposed methods, ultrasound measurement for muscle pennation angles can be more widely used for functional assessment of muscles.     

Computational methods for quantifying in vivo muscle fascicle curvature from ultrasound images

Muscle fascicles curve during contraction, and this has been seen using B-mode ultrasound. Curvature can vary along a fascicle, and amongst the fascicles within a muscle. The purpose of this study was to develop an automated method for quantifying curvature across the entirety of an imaged muscle, to test the accuracy of the method against synthetic images of known curvature and noise, and to test the sensitivity of the method to ultrasound probe placement. Both synthetic and ultrasound images were processed using multiscale vessel enhancement filtering to accentuate the muscle fascicles, wavelet-based methods were used to quantify fascicle orientations and curvature distribution grids were produced by quantifying local curvatures for each point within the image. Ultrasound images of ramped isometric contractions of the human medial gastrocnemius were acquired in a test–retest study.The methods enabled distinct curvatures to be determined in different regions of the muscle. The methods were sensitive to kernel sizes during image processing, noise within the image and the variability of probe placements during retesting. Across the physiological range of curvatures and noise, curvatures calculated from validation grids were quantified with a typical standard error of less than 0.026 m^?1, and this is about 1% of the maximum curvatures observed in fascicles of contracting muscle.     

Reliability and robustness of muscle architecture measurements obtained using diffusion tensor imaging with anatomically constrained tractography

For detailed analyses of muscle adaptation mechanisms during growth, ageing or disease, reliable measurements of muscle architecture are required. Diffusion tensor imaging (DTI) and DTI tractography have been used to reconstruct the architecture of human muscles in vivo. However, muscle architecture measurements reconstructed with conventional DTI techniques are often anatomically implausible because the reconstructed fascicles do not terminate on aponeuroses, as real muscle fascicles are known to do. In this study, we tested the reliability of an anatomically constrained DTI-based method for measuring three-dimensional muscle architecture. Anatomical magnetic resonance images and diffusion tensor images were obtained from the left legs of eight healthy participants on two occasions one week apart. Muscle volumes, fascicle lengths, pennation angles and fascicle curvatures were measured in the medial and lateral gastrocnemius, soleus and the tibialis anterior muscles. Averaged across muscles, the intraclass correlation coefficient was 0.99 for muscle volume, 0.81 for fascicle length, 0.73 for pennation angle and 0.76 for fascicle curvature. Measurements of muscle architecture obtained using conventional DTI tractography were highly sensitive to variations in the stopping criteria for DTI tractography. The application of anatomical constraints reduced this sensitivity significantly. This study demonstrates that anatomically constrained DTI tractography can provide reliable and robust three-dimensional measurements of whole-muscle architecture. The algorithms used to constrain tractography have been made publicly available.     

Three-dimensional analysis of the arrangement and length distribution of fascicles in the triceps muscle of Galea musteloides (Rodentia, Cavimorpha)

Non-uniformity of fascicle parameters (fascicle lengths and orientation) within one skeletal muscle is well known. These parameters have an effect on the physiological cross-sectional area and lengthening rate of the skeletal muscle. Using a binocular microscope with a table driver (q- and p-axes) and vertical drive (v-axis) as a tool for reconstruction of the spatial orientation of single muscle fascicles, we developed an approach for three-dimensional analysis of the arrangement and length distribution in the skeletal muscle of small mammals. Two subunits of the triceps brachii muscle of the Galea musteloides forelimb, triceps longum and triceps laterale, were quantified and compared. Our data show that in the triceps laterale the fascicles are significantly longer (10.23 mm, SD=1.19, n=41) than those in the triceps longum (6.58 mm, SD=2.88, n=39). In the triceps laterale, the fascicle orientation is more or less uniform, whereas, in the triceps longum, there are two areas with different orientation of fascicles: anterior and posterior ones. Different inner architecture of the subunits can be interpreted as an adaptation to the main locomotory function of the triceps muscle, namely production of propulsive force during limb transfer phase and keeping dynamic stability during stance phase. Comparison of our data on the fascicle length and geometry with our previous histochemical results on G. musteloides, shows that the anterior region of the triceps longum, which differs in the fascicle orientation, also contains a significantly larger percent of slow muscle fibres. It is hypothesised here that this small region is involved in keeping posture. Accepted: 16 May 2000     

In vivo fascicle length measurements via B-mode ultrasound imaging with single vs dual transducer arrangements

Ultrasonography is a useful technique to study muscle contractions in vivo, however larger muscles like vastus lateralis may be difficult to visualise with smaller, commonly used transducers. Fascicle length is often estimated using linear trigonometry to extrapolate fascicle length to regions where the fascicle is not visible. However, this approach has not been compared to measurements made with a larger field of view for dynamic muscle contractions. Here we compared two different single-transducer extrapolation methods to measure VL muscle fascicle length to a direct measurement made using two synchronised, in-series transducers. The first method used pennation angle and muscle thickness to extrapolate fascicle length outside the image (extrapolate method). The second method determined fascicle length based on the extrapolated intercept between a fascicle and the aponeurosis (intercept method). Nine participants performed maximal effort, isometric, knee extension contractions on a dynamometer at 10° increments from 50 to 100° of knee flexion. Fascicle length and torque were simultaneously recorded for offline analysis. The dual transducer method showed similar patterns of fascicle length change (overall mean coefficient of multiple correlation was 0.76 and 0.71 compared to extrapolate and intercept methods respectively), but reached different absolute lengths during the contractions. This had the effect of producing force–length curves of the same shape, but each curve was shifted in terms of absolute length. We concluded that dual transducers are beneficial for studies that examine absolute fascicle lengths, whereas either of the single transducer methods may produce similar results for normalised length changes, and repeated measures experimental designs.     

A 3D model of muscle reveals the causes of nonuniform strains in the biceps brachii

Biomechanical models generally assume that muscle fascicles shorten uniformly. However, dynamic magnetic resonance (MR) images of the biceps brachii have recently shown nonuniform shortening along some muscle fascicles during low-load elbow flexion (J. Appl. Physiol. 92 (2002) 2381). The purpose of this study was to uncover the features of the biceps brachii architecture and material properties that could lead to nonuniform shortening. We created a three-dimensional finite-element model of the biceps brachii and compared the tissue strains predicted by the model with experimentally measured tissue strains. The finite-element model predicted strains that were within one standard deviation of the experimentally measured strains. Analysis of the model revealed that the variation in fascicle lengths within the muscle and the curvature of the fascicles were the primary factors contributing to nonuniform strains. Continuum representations of muscle, combined with in vivo image data, are needed to deepen our understanding of how complex geometric arrangements of muscle fibers affect muscle contraction mechanics.     

Demonstration of extended field-of-view ultrasound’s potential to increase the pool of muscles for which in vivo fascicle length is measurable

Static, B-mode ultrasound is the most common method of measuring fascicle length in vivo. However, most forearm muscles have fascicles that are longer than the field-of-view of traditional ultrasound (T-US). As such, little work has been done to quantify in vivo forearm muscle architecture. The extended field-of-view ultrasound (EFOV-US) method, which fits together a sequence of B-mode images taken from a continuous ultrasound scan, facilitates direct measurements of longer, curved fascicles. Here, we test the validity and reliability of the EFOV-US method for obtaining fascicle lengths in the extensor carpi ulnaris (ECU). Fascicle lengths from images of the ECU captured in vivo with EFOV-US were compared to lengths from a well-established method, T-US. Images were collected in a joint posture that shortens the ECU such that entire fascicle lengths were captured within a single T-US image. Resulting measurements were not significantly different (p = 0.18); a Bland-Altman test demonstrated their agreement. A novice sonographer implemented EFOV-US in a phantom and in vivo on the ECU. The novice sonographer’s measurements from the ultrasound phantom indicate that the combined imaging and analysis method is valid (average error = 2.2 ± 1.3 mm) and the in vivo fascicle length measurements demonstrate excellent reliability (ICC = 0.97). To our knowledge, this is the first study to quantify in vivo fascicle lengths of the ECU using any method. The ability to define a muscle’s architecture in vivo using EFOV-US could lead to improvements in diagnosis, model development, surgery guidance, and rehabilitation techniques.     

Changes in human skeletal muscle architecture and function induced by extended spaceflight

The aim of this study was to quantitatively describe the relationships between joint angles and muscle architecture (lengths (L_f) and angles (Θ_f) of fascicles) of human triceps surae [medial (MG) and lateral (LG) gastrocnemius and soleus (SOL) muscles] in vivo for three men-cosmonaut after long-duration spaceflight. Sagittal sonographs of MG, LG, SOL were taken at ankle was positioned at 15° (dorsiflexion), 0° (neutral position), +15°, and +30° (plantarflexion), with the knee at 90° at rest and after a long-duration spaceflight. At each position, longitudinal ultrasonic images of the MG and LG and SOL were obtained while the cosmonauts was relaxed from which fascicle lengths and angles with respect to the aponeuroses were determined. After space flight plantarflexor force declined significantly (26%; p < 0.001). The internal architecture of the GM, and LG, and SOL muscle was significantly altered. In the passive condition, L_f changed from 45, 53, and 39 mm (knee, 0°, ankle, −15°) to 26, 33, and 28 mm (knee, 90° ankle, 30°) for MG, LG, and SOL, respectively. Different lengths and angles of fascicles, and their changes by contraction, might be related to differences in force-producing capabilities of the muscles and elastic characteristics of tendons and aponeuroses. The three heads of the triceps surae muscle substantially differ in architecture, which probably reflects their functional roles. Differences in fiber length and pennation angle that were observed among the muscles and could be associated with differences in force production and in elastic properties of musculo-tendinous complex and aponeuroses.     

Passive knee movement-induced modulation of the soleus H-reflex and alteration in the fascicle length of the medial gastrocnemius muscle in humans

In humans, an inhibitory via Ia afferent pathway from the medial gastrocnemius (MG) to the soleus (SOL) motoneuron pool has been suggested. Herein, we examined the relation between MG fascicle length changes and the SOL H-reflex modulation during passive knee movement. Twelve subjects performed static and passive (5° s^?1) knee movement tasks with the ankle immobilized using an isokinetic dynamometer in sitting posture. The maximal H- and M-waves were measured at four target angles (20°, 40°, 60°, and 80° flexion from full knee extension). The MG fascicles length and velocity were measured using a B-mode ultrasonic apparatus. Results demonstrated that the SOL Hmax/Mmax; i.e., ratio of the maximal H- to M-waves, was attenuated with increasing MG fascicle length in static tasks. The SOL Hmax/Mmax at 20° was significantly attenuated compared with 60° and 80° with increasing MG fascicle length and lengthening velocity in passive knee extension. However, no significant differences in the SOL Hmax/Mmax were found across the target angles in the passive knee flexion task. In conclusion, as muscle spindles increase their discharge with lengthening fascicle velocity, but keep silent when fascicles shorten, our data suggest that lengthening the MG facilitates an inhibitory Ia pathway from MG to SOL, and modulates SOL motoneuron activity during movements.     

Lateral force transmission between human tendon fascicles.

Whether adjacent collagen fascicles transmit force in parallel is unknown. The purpose of the present study was to examine the magnitude of lateral force transmission between adjacent collagen fascicles from the human patellar and Achilles tendon. From each sample two adjacent strands of fascicles (phi 300-530 mum) enclosed in a fascicular membrane were dissected. The specimen was deformed to approximately 3% strain in three independent load-displacement cycles in a small-scale tensile testing device. Cycle 1: the fascicles and the fascicular membrane were intact. Cycle 2: one fascicle was transversally cut while the other fascicle and the fascicular membrane were kept intact. Cycle 3: both fascicles were cut in opposite ends while the fascicular membrane was left intact. A decline in peak force of 45% and 55% from cycle 1 to cycle 2, and 93% and 92% from cycle 2 to cycle 3 was observed in the patellar and Achilles tendon fascicles, respectively. A decline in stiffness of 39% and 60% from cycle 1 to cycle 2, and of 93% and 100% from cycle 2 to cycle 3 was observed in the patellar and Achilles tendon fascicles, respectively. The present data demonstrate that lateral force transmission between adjacent collagen fascicles in human tendons is small or negligible, suggesting that tendon fascicles largely act as independent structures and that force transmission principally takes place within the individual fascicles.     

Quantification of trabecular spatial orientation from low-resolution images

No accepted methodology exists to assess trabecular bone orientation from clinical CT scans. The aim of this study was to test the hypothesis that the distribution of grey values in clinical CT images is related to the underlying trabecular architecture and that this distribution can be used to identify the principal directions and local anisotropy of trabecular bone. Fourteen trabecular bone samples were extracted from high-resolution (30 μm) micro-CT scans of seven human femoral heads. Trabecular orientations and local anisotropy were calculated using grey-level deviation (GLD), a novel method providing a measure of the three-dimensional distribution of image grey values. This was repeated for different image resolutions down to 300 μm and for volumes of interest (VOIs) ranging from 1 to 7 mm. Outcomes were compared with the principal mechanical directions and with mean intercept length (MIL) as calculated for the segmented 30-μm images. For the 30-μm images, GLD predicted the mechanical principal directions equally well as MIL. For the 300-μm images, which are resolutions that can be obtained in vivo using clinical CT, only a small increase (3°–6°) in the deviation from the mechanical orientations was found. VOIs of 5 mm resulted in a robust quantification of the orientation. We conclude that GLD can quantify structural bone parameters from low-resolution CT images.     

Myofascial force transmission between the human soleus and gastrocnemius muscles during passive knee motion

The plantarflexors of the lower limb are often assumed to act as independent actuators, but the validity of this assumption is the subject of considerable debate. This study aims to determine the degree to which passive changes in gastrocnemius muscle length, induced by knee motion, affect the tension in the adjacent soleus muscle. A second aim is to quantify the magnitude of myofascial passive force transmission between gastrocnemius and adjacent soleus. Fifteen healthy volunteers participated. Simultaneous ultrasound images of the gastrocnemius and soleus muscles were obtained during passive knee flexion (0-90°), while keeping the ankle angle fixed at either 70° or 115°. Image correlation analysis was used to quantify muscle fascicle lengths in both muscles. The data show that the soleus muscle fascicles elongate significantly during gastrocnemius shortening. The approximate change in passive soleus force as a result of the observed change in fascicle length was estimated and appears to be <5 N, but this estimate is sensitive to the assumed slack length of soleus.     

Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running

Ultrasound imaging has recently been used to distinguish the length changes of muscle fascicles from those of the whole muscle tendon complex during real life movements. The complicated three-dimensional architecture of pennate muscles can however cause heterogeneity in the length changes along the length of a muscle. Here we use ultrasonography to examine muscle fascicle length and pennation angle changes at proximal, distal and midbelly sites of the human gastrocnemius medialis (GM) muscle during walking (4.5 km/h) and running (7.5 km/h) on a treadmill. The results of this study have shown that muscle fascicles perform the same actions along the length of the human GM muscle during locomotion. However the distal fascicles tend to shorten more and act at greater pennation angles than the more proximal fascicles. Muscle fascicles acted relatively isometrically during the stance phase during walking, however during running the fascicles shortened throughout the stance phase, which corresponded to an increase in the strain of the series elastic elements (SEEs) (consisting of the Achilles tendon and aponeurosis). Measurement of the fascicle length changes at the midbelly level provided a good approximation of the average fascicle length changes across the length of the muscle. The compliance of the SEE allows the muscle fascicles to shorten at a much slower speed, more concomitant with their optimal speed for maximal power output and efficiency, with high velocity shortening during take off in both walking and running achieved by recoil of the SEE.     

Muscle fiber and tendon length changes in the human vastus lateralis during slow pedaling.

Muscle fascicle lengths of vastus lateralis (VL) muscle were measured in five healthy men during slow pedaling to investigate the interaction between muscle fibers and tendon. Subjects cycled at a pedaling rate of 40 rpm (98 W). During exercise, fascicle lengths changed from 91 +/- 7 (SE) to 127 +/- 5 mm. It was suggested that fascicles were on the descending limb of their force-length relationship. The average shortening velocity of fascicle was greater than that of muscle-tendon complex in the first half of the knee extension phase and was less in the second half. The maximum shortening velocity of fascicle in the knee extension phase was less than that of muscle-tendon complex by 22 +/- 9%. These discrepancies in velocities were mainly caused by the elongation of the tendinous tissue. It was suggested that the elasticity of VL tendinous tissue enabled VL fascicles to develop force at closer length to their optimal length and kept the maximum shortening velocity of VL fascicles low during slow pedaling.     

In vivo operational fascicle lengths of vastus lateralis during sub-maximal and maximal cycling

Instantaneous contractile characteristics of skeletal muscle, during movement tasks, can be determined and related to steady state mechanical properties such as the force–length relationship with the use of ultrasound imaging. A previous investigation into the contractile characteristics of the vastus lateralis (VL) during cycling has shown that fascicles operate on the “weak” descending limb of the force–length relationship, thus not taking advantage of the “strong” plateau region. The purpose of this study was to investigate if VL fascicle lengths change from sub-maximal to maximal cycling conditions, and if maximal cycling results in VL fascicle lengths which operate across the plateau of the force–length relationship. Fifteen healthy male subjects (age 20.9±1.8 yr, wt. 67.0±6.3 kg, ht. 176.7±7.2 cm) were tested to establish the maximal force–length relationship for the VL through ten maximal isometric contractions at various knee angles. Subjects then cycled on an SRM cycle ergometer at cadences of 50 and 80 revolutions per minute at 100 W, 250 W, and maximal effort. Fascicle lengths were determined at crank angles of 0, 90, and 180°. Fascicles operated at or near the plateau of the maximal force–length relationship for maximal cycling, while operating on the descending limb during sub-maximal conditions for both cadences. However, when comparing the fascicle operating range for the sub-maximal cycling conditions to the corresponding sub-maximal force–length relationships, the VL now also operated across the plateau region. We concluded from these results that regardless of cycling effort, the VL operated through the ideal plateau region of the corresponding force–length relationship, hence always working optimally. We hypothesize that this phenomenon is due to the coupling of series elastic compliance and length dependent calcium sensitivity in the VL.     

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.     

Left septal fascicular block: myth or reality?

Anatomic studies have shown that the left bundle branch divides into three fascicles in most humans. Changes in the 12 lead ECG (electrocardiogram) due to conduction abnormalities of the left anterior fascicle and left posterior fascicle are now part of the standard repertoire of electrocardiographic interpretation. There are no standard criteria for detecting conduction defects involving the third left fascicle, the septal or median fascicle, and the very existence of such defects is still a matter of controversy. The purposes of this article are to review the available evidence on this subject, suggest electrocardiographic criteria for its recognition, and present examples which illustrate that left septal fascicular block does indeed exist as a specific entity. Left septal fascicular block is a polymorphic conduction defect which may explain some previously inadequately understood electrocardiographic abnormalities.     

Heterogeneous fascicle behavior within the biceps femoris long head at different muscle activation levels

Magnetic resonance and ultrasound imaging have shown hamstring strain injuries occur most often in the biceps femoris long head (BFLH), and particularly in the proximal vs. distal region of this muscle. Animal research and musculoskeletal modeling (MSK) have detected heterogeneous fascicle behavior within muscle regions, and within fascicles. Understanding architectural behavior differences during muscle contractions may help to discern possible mechanisms behind proximal BFLH injuries. The purpose of our study was to assess the magnitude of shortening of the proximal and distal fascicles of the BFLH under a range of muscle activation levels under isometric conditions using ultrasound imaging (US). Thirteen healthy adults performed targeted sustained isometric contractions while US were taken of the entire BFLH. Measurements of fascicle lengths in both muscle regions were compared at 20%, 30%, 50%, and 67% MVIC. The results showed that while both regions shortened significantly with activation, the proximal fascicles were significantly longer, regardless of activation level (~38%), and shortened significantly more than the distal fascicles overall (~40%), and cumulatively at higher activation levels (30% and above). No significant strain differences were found between the two regions. These data suggest heterogeneous fascicle behavior exists in an absolute sense; however, differences in behavior are eliminated when normalized (strain). Coupled with MSK literature, the absence of regional fascicle strain differences in this study may indicate strain heterogeneity is not detectable at the whole fascicle level. Further knowledge of this commonly strained muscle?s regional behavior during dynamic movements could provide evidence of proximal hamstring strain predisposition.     

Changes of calf muscle-tendon biomechanical properties induced by passive-stretching and active-movement training in children with cerebral palsy

Biomechanical properties of calf muscles and Achilles tendon may be altered considerably in children with cerebral palsy (CP), contributing to childhood disability. It is unclear how muscle fascicles and tendon respond to rehabilitation and contribute to improvement of ankle-joint properties. Biomechanical properties of the calf muscle fascicles of both gastrocnemius medialis (GM) and soleus (SOL), including the fascicle length and pennation angle in seven children with CP, were evaluated using ultrasonography combined with biomechanical measurements before and after a 6-wk treatment of passive-stretching and active-movement training. The passive force contributions from the GM and SOL muscles were separated using flexed and extended knee positions, and fascicular stiffness was calculated based on the fascicular force-length relation. Biomechanical properties of the Achilles tendon, including resting length, cross-sectional area, and stiffness, were also evaluated. The 6-wk training induced elongation of muscle fascicles (SOL: 8%, P = 0.018; GM: 3%, P = 0.018), reduced pennation angle (SOL: 10%, P = 0.028; GM: 5%, P = 0.028), reduced fascicular stiffness (SOL: 17%, P = 0.128; GM: 21%, P = 0.018), decreased tendon length (6%, P = 0.018), increased Achilles tendon stiffness (32%, P = 0.018), and increased Young's modulus (20%, P = 0.018). In vivo characterizations of calf muscles and Achilles tendon mechanical properties help us better understand treatment-induced changes of calf muscle-tendon and facilitate development of more effective treatments.