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.     

Finite element modeling reveals complex strain mechanics in the aponeuroses of contracting skeletal muscle

A finite element model was used to investigate the counter-intuitive experimental observation that some regions of the aponeuroses of a loaded and contracting muscle may shorten rather than undergo an expected lengthening. The model confirms the experimental findings and suggests that pennation angle plays a significant role in determining whether regions of the aponeuroses stretch or shorten. A smaller pennation angles (25°) was accompanied by aponeurosis lengthening whereas a larger pennation angle (47°) was accompanied by mixed strain effects depending upon location along the length of the aponeurosis. This can be explained by the Poisson effect during muscle contraction and a Mohr’s circle analogy. Constant volume constraint requires that fiber cross sectional dimensions increase when a fiber shortens. The opposing influences of these two strains upon the aponeurosis combine in proportion to the pennation angle. Lower pennation angles emphasize the influence of fiber shortening upon the aponeurosis and thus favor aponeurosis compression, whereas higher pennation angles increase the influence of cross sectional changes and therefore favor aponeurosis stretch. The distance separating the aponeuroses was also found to depend upon pennation angle during simulated contractions. Smaller pennation angles favored increased aponeurosis separation larger pennation angles favored decreased separation. These findings caution that measures of the mechanical properties of aponeuroses in intact muscle may be affected by contributions from adjacent muscle fibers and that the influence of muscle fibers on aponeurosis strain will depend upon the fiber pennation angle.     

Can pennation angles be predicted from EMGs for the primary ankle plantar and dorsiflexors during isometric contractions?

Ultrasonography was used to measure pennation angle and electromyography (EMG) to record muscle activity of the human tibialis anterior (TA), lateral gastrocnemius (LG), medial gastrocnemius (MG), and soleus (SOL) muscles during graded isometric ankle plantar and dorsiflexion contractions done on a Biodex dynamometer. Data from 8 male and 8 female subjects were collected in increments of approximately 25% of maximum voluntary contraction (MVC) ranging from rest to MVC. A significant positive linear relationship (p<0.05) between normalized EMG and pennation angle for all muscles was observed when subject specific pennation angles at rest and MVC were included in the analysis. These were included to account for gender differences and inter-subject variability in pennation angle. The coefficient of determination, R(2), ranged between 0.76 for the TA and 0.87 for the SOL. The EMG-pennation angle relationships have ramifications for use in EMG-driven models of muscle force. The regression equations can be used to characterize fiber pennation angle more accurately and to determine how it changes with contraction intensity, thus providing improved estimates of muscle force when using musculoskeletal models.     

Anisotropic Smoothing Improves DT-MRI-Based Muscle Fiber Tractography

Purpose

To assess the effect of anisotropic smoothing on fiber tracking measures, including pennation angle, fiber tract length, and fiber tract number in the medial gastrocnemius (MG) muscle in healthy subjects using diffusion-weighted magnetic resonance imaging (DW-MRI).

Materials and Methods

3T DW-MRI data were used for muscle fiber tractography in the MG of healthy subjects. Anisotropic smoothing was applied at three levels (5%, 10%, 15%), and pennation angle, tract length, fiber tract number, fractional anisotropy, and principal eigenvector orientation were quantified for each smoothing level.

Results

Fiber tract length increased with pre-fiber tracking smoothing, and local heterogeneities in fiber direction were reduced. However, pennation angle was not affected by smoothing.

Conclusion

Modest anisotropic smoothing (10%) improved fiber-tracking results, while preserving structural features.     

Load-dependent Variable Gearing Mechanism of Muscle-like Soft Actuator

Pennate muscle is characterized by muscle fibers that are oriented at a certain angle(pennation angle)relative to the muscle's line of action and rotation durin...     

Optimal pennation angle of the primary ankle plantar and dorsiflexors: variations with sex, contraction intensity, and limb

Ultrasonography was used to measure the pennation angle of the human tibialis anterior (TA), lateral gastrocnemius (LG), medial gastrocnemius (MG), and soleus (Sol). The right and left legs of 8 male and 8 female subjects were tested at rest and during maximum voluntary contraction (MVC). Joint angles were chosen to control muscle tendon lengths so that the muscles were near their optimal length within the length-tension relationship. No differences in pennation angle were detected between the right and left legs. Another consistent finding was that the pennation angle at MVC was significantly greater than at rest for all muscles tested. Optimal pennation angles for the TA, MG, and Sol were significantly greater for the men than for the women. Optimal pennation angles for the TA, LG, MG, and Sol for the male subjects were 14.3 degrees, 23.7 degrees, 34.6 degrees, and 40.1 degrees respectively, whereas values of 12.1 degrees, 16.3 degrees, 27.3 degrees, and 26.3 degrees were recorded for the female subjects. The results of this study suggest the following: (1) similar values for pennation angle can be used for the right and left TA, LG, MG, and Sol; (2) pennation angle is significantly greater at MVC than at rest for all muscles tested; and (3) sex-specific values for optimal pennation angle should be used when modeling the force-generating potential of the primary muscles responsible for ankle plantar and dorsiflexion.     

Predictability of in vivo changes in pennation angle of human tibialis anterior muscle from rest to maximum isometric dorsiflexion

The aim of this study was to assess the predictability of in vivo, ultrasound-based changes in human tibialis anterior (TA) pennation angle from rest to maximum isometric dorsiflexion (MVC) using a planimetric model assuming constant thickness between aponeuroses and straight muscle fibres. Sagittal sonographs of TA were taken in six males at ankle angles of -15 degrees (dorsiflexion direction), 0 degrees (neutral position), + 15 (plantarflexion direction) and + 30 degrees both at rest and during dorsiflexor MVC trials performed on an isokinetic dynamometer. At all four ankle angles scans were taken from the TA proximal, central and distal regions. TA architecture did not differ (P > 0.05) neither between its two unipennate parts nor along the scanned regions over its length at a given ankle angle and state of contraction. Comparing MVC with rest at any given ankle angle, pennation angle was larger (62-71%, P < 0.01), fibre length smaller (37-40%, P < 0.01) and muscle thickness unchanged (P > 0.05). The model used estimated accurately (P > 0.05) changes in TA pennation angle occurring in the transition from rest to MVC and therefore its use is encouraged for estimating the isometric TA ankle moment and force generating capacity using musculoskeletal modelling.     

Pennation angles of the intrinsic muscles of the foot

As mathematical models of the musculoskeletal system become increasingly detailed and precise, they require more accurate information about the architectural parameters of the individual muscles. These muscles are typically represented as Hill-type models, which require data on fiber length, physiological cross-sectional area (PCSA) and pennation angle. Most of this information for lower limb muscles has been published, except for data on the pennation angle of the intrinsic muscles of the foot. Each (n=20) intrinsic muscle of three human feet was dissected free. The dorsal and plantar surfaces were photographed and a digitized color image was imported into Abobe Photoshop. The muscles were divided into "anatomical units". For each anatomical unit (n=26), a line was drawn along the tendon axis and a number of other lines were drawn along individual muscle fibers. The angle between the tendon line and each fiber line was defined as the pennation angle of that fiber. By visual inspection, an effort was made to take measurements such that they represented the distribution of fibers in various parts of the muscle. Although some individual muscles had higher or lower pennation angles, when averaged for all specimens, the second dorsal interosseous had the smallest pennation angle (6.7+/-6.81 degrees) while the abductor digiti minimi had the largest (19.1+/-11.19 degrees). Since the cosines of the angles range from 0.9932 to 0.9449, the effect of the pennation angle on the force generated by the muscle was not great.     

In vivo specific tension of human skeletal muscle.

In this study, we estimated the specific tensions of soleus (Sol) and tibialis anterior (TA) muscles in six men. Joint moments were measured during maximum voluntary contraction (MVC) and during electrical stimulation. Moment arm lengths and muscle volumes were measured using magnetic resonance imaging, and pennation angles and fascicular lengths were measured using ultrasonography. Tendon and muscle forces were modeled. Two approaches were followed to estimate specific tension. First, muscle moments during electrical stimulation and moment arm lengths, fascicular lengths, and pennation angles during MVC were used (data set A). Then, MVC moments, moment arm lengths at rest, and cadaveric fascicular lengths and pennation angles were used (data set B). The use of data set B yielded the unrealistic specific tension estimates of 104 kN/m(2) in Sol and 658 kN/m(2) in TA. The use of data set A, however, yielded values of 150 and 155 kN/m(2) in Sol and TA, respectively, which agree with in vitro results from fiber type I-predominant muscles. In fact, both Sol and TA are such muscles. Our study demonstrates the feasibility of accurate in vivo estimates of human muscle intrinsic strength.     

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.     

The effect of ultrasound probe orientation on muscle architecture measurement.

The purpose of this paper was to examine how muscle architecture parameter (MAP) measurements made using brightness-mode ultrasonography (BMU) differ based on probe orientation. The human tibialis anterior muscle was imaged from nine different probe orientations during concentric contractions at four joint angles to determine the effect of probe orientation on the measurement of muscle architecture parameters. Ankle dorsi-flexion torque, tibialis anterior electromyography (EMG), and measures of MAP including fascicle length (FL), pennation angle (PA) and muscle thickness (MT) were collected. Statistically significant differences were found between joint angles for measures of FL and PA and between probe orientations for measures of FL and MT. A comparison of actual MAP values to a geometric model used by researchers to determine an ideal probe orientation show that the actual values vary to a greater extent and do not follow the trend predicted by the model. The results suggest that ultrasound probe orientation affects measures of MAP but the effect either cannot be predicted from a geometric model and/or the error in the measurement technique does not allow a comparison.     

Reproducibility of gastrocnemius medialis muscle architecture during treadmill running

The purpose of this study was to assess the reproducibility of fascicle length (FL) and pennation angle (PA) of gastrocnemius medialis (GM) muscle during running in vivo. Twelve male recreational long distance runners (mean ± SD; age: 24 ± 3 years, mass: 76 ± 7 kg) ran on a treadmill at a speed of 3.0 m/s, wearing their own running shoes, for two different 10 min sessions that were at least 2 days apart. For each test day 10 acceptable trials were recorded. Ankle and knee joint angle data were recorded by a Vicon 624 system with three cameras operating at 120 Hz. B-mode ultrasonography was used to examine fascicle length and pennation angle of gastrocnemius medialis muscle. The ultrasound probe was firmly secured on the muscle belly using a lightweight foam fixation. The results indicated that fascicle length and pennation angle demonstrated high reproducibility values during treadmill running both for within and between test days. The root mean square scores between the repeated waveforms of pennation angle and fascicle length were small (∼2° and ∼3.5 mm, respectively). However, ∼14 trials for pennation angle and ∼9 trials for fascicle length may be required in order to record accurate data from muscle architecture parameters. In conclusion, ultrasound measurements may be highly reproducible during dynamic movements such as treadmill running, provided that a proper fixation is used in order to assure the constant location and orientation of the ultrasound probe throughout the movement.     

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.     

Changes in fascicle lengths and pennation angles do not contribute to residual force enhancement/depression in voluntary contractions

Force enhancement following muscle stretching and force depression following muscle shortening are well-accepted properties of skeletal muscle contraction. However, the factors contributing to force enhancement/depression remain a matter of debate. In addition to factors on the fiber or sarcomere level, fiber length and angle of pennation affect the force during voluntary isometric contractions in whole muscles. Therefore, we hypothesized that differences in fiber lengths and angles of pennation between force-enhanced/depressed and reference states may contribute to force enhancement/depression during voluntary contractions. The purpose of this study was to test this hypothesis. Twelve subjects participated in this study, and force enhancement/depression was measured in human tibialis anterior. Fiber lengths and angles of pennation were quantified using ultrasound imaging. Neither fiber lengths nor angles of pennation were found to differ between the isometric reference contractions and any of the force-enhanced or force-depressed conditions. Therefore, we rejected our hypothesis and concluded that differences in fiber lengths or angles of pennation do not contribute to the observed force enhancement/depression in human tibialis anterior, and speculate that this result is likely true for other muscles too.     

Determining skeletal muscle architecture with Laplacian simulations: a comparison with diffusion tensor imaging

Determination of skeletal muscle architecture is important for accurately modeling muscle behavior. Current methods for 3D muscle architecture determination can be costly and time-consuming, making them prohibitive for clinical or modeling applications. Computational approaches such as Laplacian flow simulations can estimate muscle fascicle orientation based on muscle shape and aponeurosis location. The accuracy of this approach is unknown, however, since it has not been validated against other standards for muscle architecture determination. In this study, muscle architectures from the Laplacian approach were compared to those determined from diffusion tensor imaging in eight adult medial gastrocnemius muscles. The datasets were subdivided into training and validation sets, and computational fluid dynamics software was used to conduct Laplacian simulations. In training sets, inputs of muscle geometry, aponeurosis location, and geometric flow guides resulted in good agreement between methods. Application of the method to validation sets showed no significant differences in pennation angle (mean difference \(0.5{^{\circ }})\) or fascicle length (mean difference 0.9 mm). Laplacian simulation was thus effective at predicting gastrocnemius muscle architectures in healthy volunteers using imaging-derived muscle shape and aponeurosis locations. This method may serve as a tool for determining muscle architecture in silico and as a complement to other approaches.     

Human gastrocnemius medialis pennation angle as a function of age: from newborn to the elderly.

The aim of the present study was to quantify changes in human skeletal muscle pennation angle (F theta) values during growth and adult life. The human gastrocnemius medialis muscle of 162 subjects (96 males and 66 females) in the age range 0-70 years was scanned with ultrasonography. The subjects were laying prone, at rest, with the ankle maintained at 90 degrees with all muscles relaxed. F theta increased monotonically starting from birth (0 years) and reached a stable value after the adolescent growth spurt. There was a significant (p < 0.05) linear relationship between F theta and muscle thickness (TK). F theta = 0.84 (+/- 0.09) * TK + 3.15 (+/- 1.13). Human gastrocnemius medialis F theta and TK data found in the literature seem to fit the F theta-TK plot in a coherent manner, independent of the physiological or anatomical characteristics of the subject. The present findings indicate that F theta is not a constant parameter but evolves, as is the case for bone length and height, as a function of age.     

Determination of fascicle length and pennation in a contracting human muscle in vivo

Fukunaga, Tetsuo, Yoshiho Ichinose, Masamitsu Ito, YasuoKawakami, and Senshi Fukashiro. Determination of fascicle lengthand pennation in a contracting human muscle in vivo.J. Appl. Physiol. 82(1): 354-358, 1997.We have developed a technique to determine fascicle length inhuman vastus lateralis muscle in vivo by using ultrasonography. Whenthe subjects had the knee fully extended passively from a position of110° flexion (relaxed condition), the fascicle length decreasedfrom 133 to 97 mm on average. During static contractions at 10% ofmaximal voluntary contraction strength (tensed condition), fascicleshortening was more pronounced (from 126 to 67 mm), especially when theknee was closer to full extension. Similarly, as the knee was extended, the angle of pennation (fascicle angle, defined as the angle between fascicles and aponeurosis) increased (relaxed, from 14 to 18°; tensed, from 14 to 21°), and a greater increase in the pennation angle was observed in the tensed than in the relaxed condition when theknee was close to extension (<40°). We conclude that there aredifferences in fascicle lengths and pennation angles when the muscle isin a relaxed and isometrically tensed conditions and that thedifferences are affected by joint angles, at least at thesubmaximal contraction level.

     

The isometric length-force models of nine different skeletal muscles.

The length-force relations of nine different skeletal muscles in the hindlimb of the cat were determined experimentally, with electrical stimulation of the sciatic nerve as the activation mode. It was shown that the active-, passive-, and total-force patterns varied widely among the muscles. The tibialis posterior (TP), medial and lateral gastrocnemius (MG, LG) and flexor digitorum longus (FDL) had a symmetric active-force curve, whereas the tibialis anterior (TA), peroneus brevis (PB), peroneus longus (PL), extensor digitorum longus (EDL), and soleus (SOL) had an asymmetric curve which exhibits about 25% of the maximal isometric force at extreme lengths. The SOL, EDL, and LG had a low-level passive force which appeared at short muscle length, whereas all other muscles exhibited initial passive force just before the optimal length. The total force was rising quasi-linearly for the SOL, whereas the other muscles exhibited an intermediate plateau about the optimal length. The LG and FDL had a substantial but temporary intermediate dip in the total force as the muscle was elongated past the optimal length. The elongation range of the various muscles also varied, ranging from +/- 15 to +/- 30% of the optimal length. The elongation range was symmetric for the FDL, LG, MG, TP, SOL, and EDL, and asymmetric for the PL, PB, and TA, being -12 to + 17%, -12 to + 17%, and -35 to + 12%, respectively. Two different models which incorporate muscle architecture were successfully fitted to the experimental data of the muscles except for the MG and TA. The architecture of these two muscles is highly nonhomogeneous and contains compartments with two pennation patterns or two different optimal lengths. New models, which add spatially and temporally the individual characteristics of each compartment of the muscles, were constructed for these two muscles. The new models demonstrated high correlation to the experimental data obtained from the MG and TA. It was concluded that the length-force relation varies widely among various skeletal muscles and is probably dependent on the primary function of the muscle in the context of integrated movement; this is a manifestation of architectural factors such as fiber pennation pattern and angle, cross-sectional area, ratio of muscle to tendon length, distribution of the fiber length within the muscle and compartmental pennation.     

Measurement of fibre pennation using ultrasound in the human quadriceps in vivo.

Real-time ultrasound scanning was used to measure the angles of fibre pennation of vastus lateralis (VL) and vastus intermedius (VI) of the human quadriceps (n = 12) in vivo. The maximum isometric force and cross-sectional area of the quadriceps were also measured. With the knee at right-angles the mean fibre angles for VL and VI respectively were 0.133 (0.021) rad [7.6 degrees (1.2 degrees)] and 0.143 (0.028) rad [8.2 degrees (1.6 degrees)] [mean (SD)], which is within the range of angles measured on cadavers. The mean angle decreased in going from the contracted [VL, 0.244 rad (14 degrees); VI, 0.279 rad (16 degrees)] to the stretched [VL, 0.105 rad (6 degrees); VI, 0.122 rad (7 degrees)] position. There was a significant positive correlation between fibre angle and muscle cross-sectional area but no relationship between fibre angle and force per cross-sectional area. No increase in fibre angle was detected after 3 months strength training. We conclude that ultrasound can be used to measure pennation angles of superficial muscle groups but we could not demonstrate a relationship between pennation and force-generating capacity.