Three-dimensional geometrical changes of the human tibialis anterior muscle and its central aponeurosis measured with three-dimensional ultrasound during isometric contractions

Background.Muscles not only shorten during contraction to perform mechanical work, but they also bulge radially because of the isovolumetric constraint on muscle fibres. Muscle bulging may have important implications for muscle performance, however quantifying three-dimensional (3D) muscle shape changes in human muscle is problematic because of difficulties with sustaining contractions for the duration of anin vivoscan. Although two-dimensional ultrasound imaging is useful for measuring local muscle deformations, assumptions must be made about global muscle shape changes, which could lead to errors in fully understanding the mechanical behaviour of muscle and its surrounding connective tissues, such as aponeurosis. Therefore, the aims of this investigation were (a) to determine the intra-session reliability of a novel 3D ultrasound (3DUS) imaging method for measuringin vivohuman muscle and aponeurosis deformations and (b) to examine how contraction intensity influencesin vivohuman muscle and aponeurosis strains during isometric contractions.Methods.Participants (n= 12) were seated in a reclined position with their left knee extended and ankle at 90° and performed isometric dorsiflexion contractions up to 50% of maximal voluntary contraction. 3DUS scans of the tibialis anterior (TA) muscle belly were performed during the contractions and at rest to assess muscle volume, muscle length, muscle cross-sectional area, muscle thickness and width, fascicle length and pennation angle, and central aponeurosis width and length. The 3DUS scan involved synchronous B-mode ultrasound imaging and 3D motion capture of the position and orientation of the ultrasound transducer, while successive cross-sectional slices were captured by sweeping the transducer along the muscle.Results.3DUS was shown to be highly reliable across measures of muscle volume, muscle length, fascicle length and central aponeurosis length (ICC ≥ 0.98, CV < 1%). The TA remained isovolumetric across contraction conditions and progressively shortened along its line of action as contraction intensity increased. This caused the muscle to bulge centrally, predominantly in thickness, while muscle fascicles shortened and pennation angle increased as a function of contraction intensity. This resulted in central aponeurosis strains in both the transverse and longitudinal directions increasing with contraction intensity.Discussion.3DUS is a reliable and viable method for quantifying multidirectional muscle and aponeurosis strains during isometric contractions within the same session. Contracting muscle fibres do work in directions along and orthogonal to the muscle’s line of action and central aponeurosis length and width appear to be a function of muscle fascicle shortening and transverse expansion of the muscle fibres, which is dependent on contraction intensity. How factors other than muscle force change the elastic mechanical behaviour of the aponeurosis requires further investigation.

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Nonisometric behavior of fascicles during isometric contractions of a human muscle

Journal of Applied Physiology ◽

10.1152/jappl.1998.85.4.1230 ◽

1998 ◽

Vol 85 (4) ◽

pp. 1230-1235 ◽

Cited By ~ 143

Author(s):

Masamitsu Ito ◽

Yasuo Kawakami ◽

Yoshiho Ichinose ◽

Senshi Fukashiro ◽

Tetsuo Fukunaga

Keyword(s):

Young’S Modulus ◽

Joint Angle ◽

Young's Modulus ◽

Pennation Angle ◽

Human Muscle ◽

Isometric Contractions ◽

Fascicle Length ◽

Tendon Stiffness ◽

Tendon Elongation

Fascicle length, pennation angle, and tendon elongation of the human tibialis anterior were measured in vivo by ultrasonography. Subjects ( n = 9) were requested to develop isometric dorsiflexion torque gradually up to maximal at the ankle joint angle of 20° plantarflexion from the anatomic position. Fascicle length shortened from 90 ± 7 to 76 ± 7 (SE) mm, pennation angle increased from 10 ± 1 to 12 ± 1°, and tendon elongation increased up to 15 ± 2 mm with graded force development up to maximum. The tendon stiffness increased with increasing tendon force from 10 N/mm at 0–20 N to 32 N/mm at 240–260 N. Young’s modulus increased from 157 MPa at 0–20 N to 530 MPa at 240–260 N. It can be concluded that, in isometric contractions of a human muscle, mechanical work, some of which is absorbed by the tendinous tissue, is generated by the shortening of muscle fibers and that ultrasonography can be used to determine the stiffness and Young’s modulus for human tendons.

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Three-dimensional architecture of the whole human soleus muscle in vivo

PeerJ ◽

10.7717/peerj.4610 ◽

2018 ◽

Vol 6 ◽

pp. e4610 ◽

Cited By ~ 25

Author(s):

Bart Bolsterlee ◽

Taija Finni ◽

Arkiev D’Souza ◽

Junya Eguchi ◽

Elizabeth C. Clarke ◽

...

Keyword(s):

Soleus Muscle ◽

Diffusion Tensor ◽

Three Dimensional ◽

Muscle Length ◽

Fascicle Length ◽

Cross Sectional ◽

Quantitative Measurements ◽

Muscle Fascicle ◽

Total Muscle

Background Most data on the architecture of the human soleus muscle have been obtained from cadaveric dissection or two-dimensional ultrasound imaging. We present the first comprehensive, quantitative study on the three-dimensional anatomy of the human soleus muscle in vivo using diffusion tensor imaging (DTI) techniques. Methods We report three-dimensional fascicle lengths, pennation angles, fascicle curvatures, physiological cross-sectional areas and volumes in four compartments of the soleus at ankle joint angles of 69 ± 12° (plantarflexion, short muscle length; average ± SD across subjects) and 108 ± 7° (dorsiflexion, long muscle length) of six healthy young adults. Microdissection and three-dimensional digitisation on two cadaveric muscles corroborated the compartmentalised structure of the soleus, and confirmed the validity of DTI-based muscle fascicle reconstructions. Results The posterior compartments of the soleus comprised 80 ± 5% of the total muscle volume (356 ± 58 cm3). At the short muscle length, the average fascicle length, pennation angle and curvature was 37 ± 8 mm, 31 ± 3° and 17 ± 4 /m, respectively. We did not find differences in fascicle lengths between compartments. However, pennation angles were on average 12° larger (p < 0.01) in the posterior compartments than in the anterior compartments. For every centimetre that the muscle-tendon unit lengthened, fascicle lengths increased by 3.7 ± 0.8 mm, pennation angles decreased by −3.2 ± 0.9° and curvatures decreased by −2.7 ± 0.8 /m. Fascicles in the posterior compartments rotated almost twice as much as in the anterior compartments during passive lengthening. Discussion The homogeneity in fascicle lengths and inhomogeneity in pennation angles of the soleus may indicate a functionally different role for the anterior and posterior compartments. The data and techniques presented here demonstrate how DTI can be used to obtain detailed, quantitative measurements of the anatomy of complex skeletal muscles in living humans.

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In vivo determination of fascicle curvature in contracting human skeletal muscles

Journal of Applied Physiology ◽

10.1152/jappl.2002.92.1.129 ◽

2002 ◽

Vol 92 (1) ◽

pp. 129-134 ◽

Cited By ~ 73

Author(s):

Tadashi Muramatsu ◽

Tetsuro Muraoka ◽

Yasuo Kawakami ◽

Akira Shibayama ◽

Tetsuo Fukunaga

Keyword(s):

Maximum Voluntary Contraction ◽

Muscle Length ◽

Muscle Thickness ◽

Voluntary Contraction ◽

Pennation Angle ◽

Medial Gastrocnemius ◽

Fascicle Length ◽

Fascicle Curvature

Fascicle curvature of human medial gastrocnemius muscle (MG) was determined in vivo by ultrasonography during isometric contractions at three (distal, central, and proximal) locations ( n = 7) and at three ankle angles ( n = 7). The curvature significantly ( P < 0.05) increased from rest to maximum voluntary contraction (MVC) (0.4–5.2 m−1). In addition, the curvature at MVC became larger in the order dorsiflexed, neutral, plantar flexed ( P < 0.05). Thus both contraction levels and muscle length affected the curvature. Intramuscular differences in neither the curvature nor the fascicle length were found. The direction of curving was consistent along the muscle: fascicles were concave in the proximal side. Fascicle length estimated from the pennation angle and muscle thickness, under the assumption that the fascicle was straight, was underestimated by ∼6%. In addition, the curvature was significantly correlated to pennation angle and muscle thickness. These findings are particularly important for understanding the mechanical functions of human skeletal muscle in vivo.

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Gastrocnemius muscle specific force in boys and men

Journal of Applied Physiology ◽

10.1152/japplphysiol.00697.2007 ◽

2008 ◽

Vol 104 (2) ◽

pp. 469-474 ◽

Cited By ~ 45

Author(s):

Christopher I. Morse ◽

Keith Tolfrey ◽

Jeanette M. Thom ◽

Vasilios Vassilopoulos ◽

Constantinos N. Maganaris ◽

...

Keyword(s):

Muscle Activation ◽

Muscle Length ◽

Tanner Stage ◽

Surface Emg ◽

Specific Force ◽

Moment Arm ◽

Fascicle Length ◽

Cross Sectional ◽

Adult Men

The aim of this study was to assess whether the in vivo specific force and architectural characteristics of the lateral gastrocnemius (GL) muscle of early pubescent boys ( n = 11, age = 10.9 ± 0.3 yr, Tanner stage 2) differed from those of adult men ( n = 12, age = 25.3 ± 4.4 yr). Plantarflexor torque was 55% lower in the boys (77.4 ± 21.4 N·m) compared with the adults (175.6 ± 31.7 N·m, P < 0.01). Physiological cross-sectional area (PCSA), determined in vivo using ultrasonography and MRI, was 52% smaller in the boys ( P < 0.01). No difference was found in pennation angle, or in the ratio of fascicle length ( Lf) to muscle length between the boys and men. Moment arm length was 25% smaller in the boys ( P < 0.01). Antagonist coactivation, assessed using surface EMG on the dorsiflexors, was not different between the boys and men (11.8 ± 6.7% and 13.5 ± 5.8%, respectively). Surprisingly, GL force normalized to PCSA (specific force) was significantly higher (21%) in the boys than in the men (13.1 ± 2.0 vs. 15.9 ± 2.7 N/cm2, P < 0.05). This finding could not be explained by differences in moment arm length, muscle activation, or architecture, and other factors, such as tendinous characteristics and/or changes in moment arm length with contraction, may be held responsible. These observations warrant further investigation.

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How does passive lengthening change the architecture of the human medial gastrocnemius muscle?

Journal of Applied Physiology ◽

10.1152/japplphysiol.00976.2016 ◽

2017 ◽

Vol 122 (4) ◽

pp. 727-738 ◽

Cited By ~ 26

Author(s):

Bart Bolsterlee ◽

Arkiev D’Souza ◽

Simon C. Gandevia ◽

Robert D. Herbert

Keyword(s):

Diffusion Tensor ◽

Muscle Fibers ◽

Three Dimensional ◽

Muscle Length ◽

Muscle Architecture ◽

Medial Gastrocnemius ◽

Fascicle Length ◽

Muscle Belly ◽

Whole Muscle

There are few comprehensive investigations of the changes in muscle architecture that accompany muscle contraction or change in muscle length in vivo. For this study, we measured changes in the three-dimensional architecture of the human medial gastrocnemius at the whole muscle level, the fascicle level and the fiber level using anatomical MRI and diffusion tensor imaging (DTI). Data were obtained from eight subjects under relaxed conditions at three muscle lengths. At the whole muscle level, a 5.1% increase in muscle belly length resulted in a reduction in both muscle width (mean change −2.5%) and depth (−4.8%). At the fascicle level, muscle architecture measurements obtained at 3,000 locations per muscle showed that for every millimeter increase in muscle-tendon length above the slack length, average fascicle length increased by 0.46 mm, pennation angle decreased by 0.27° (0.17° in the superficial part and 0.37° in the deep part), and fascicle curvature decreased by 0.18 m−1. There was no evidence of systematic variation in architecture along the muscle’s long axis at any muscle length. At the fiber level, analysis of the diffusion signal showed that passive lengthening of the muscle increased diffusion along fibers and decreased diffusion across fibers. Using these measurements across scales, we show that the complex shape changes that muscle fibers, whole muscles, and aponeuroses of the medial gastrocnemius undergo in vivo cannot be captured by simple geometrical models. This justifies the need for more complex models that link microstructural changes in muscle fibers to macroscopic changes in architecture. NEW & NOTEWORTHY Novel MRI and DTI techniques revealed changes in three-dimensional architecture of the human medial gastrocnemius during passive lengthening. Whole muscle belly width and depth decreased when the muscle lengthened. Fascicle length, pennation, and curvature changed uniformly or near uniformly along the muscle during passive lengthening. Diffusion of water molecules in muscle changes in the same direction as fascicle strains.

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Behavior of human muscle fascicles during shortening and lengthening contractions in vivo

Journal of Applied Physiology ◽

10.1152/japplphysiol.01046.2002 ◽

2003 ◽

Vol 95 (3) ◽

pp. 1090-1096 ◽

Cited By ~ 136

Author(s):

Neil D. Reeves ◽

Marco V. Narici

Keyword(s):

Ankle Joint ◽

Pennation Angle ◽

Human Muscle ◽

Elastic Component ◽

Fascicle Length ◽

Series Elastic Component ◽

Muscle Fascicles ◽

Muscle Actions ◽

Series Elastic

The aim of the present study was to investigate the behavior of human muscle fascicles during dynamic contractions. Eight subjects performed maximal isometric dorsiflexion contractions at six ankle joint angles and maximal isokinetic concentric and eccentric contractions at five angular velocities. Tibialis anterior muscle architecture was measured in vivo by use of B-mode ultrasonography. During maximal isometric contraction, fascicle length was shorter and pennation angle larger compared with values at rest ( P < 0.01). During isokinetic concentric contractions from 0 to 4.36 rad/s, fascicle length measured at a constant ankle joint angle increased curvilinearly from 49.5 to 69.7 mm (41%; P < 0.01), whereas pennation angle decreased curvilinearly from 14.8 to 9.8° (34%; P < 0.01). During eccentric muscle actions, fascicles contracted quasi-isometrically, independent of angular velocity. The behavior of muscle fascicles during shortening contractions was believed to reflect the degree of stretch applied to the series elastic component, which decreases with increasing contraction velocity. The quasi-isometric behavior of fascicles during eccentric muscle actions suggests that the series elastic component acts as a mechanical buffer during active lengthening.

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Musculotendon Parameters and Musculoskeletal Pathways Within the Human Foot

Journal of Applied Biomechanics ◽

10.1123/jab.23.1.20 ◽

2007 ◽

Vol 23 (1) ◽

pp. 20-41 ◽

Cited By ~ 3

Author(s):

Melissa R. Lachowitzer ◽

Anne Ranes ◽

Gary T. Yamaguchi

Keyword(s):

Three Dimensional ◽

Pennation Angle ◽

Fascicle Length ◽

Cross Sectional ◽

Large Variability ◽

Human Foot ◽

Volume Weight ◽

Bony Landmarks ◽

Muscle Fascicle ◽

Musculoskeletal Models

In order to create a flexible model of the foot for dynamic musculoskeletal models, anthropometric data combined with geometric information describing the intrinsic musculature are needed. In this study, the left feet of two male and two female cadavers were dissected to expose the intrinsic musculotendon pathways. Three-dimensional coordinates of bony landmarks, tendon origins, insertions, and via points were digitized to submillimeter accuracy. Muscle architectural parameters were also measured, including volume, weight, and pennation angle and sarcomere, fascicle, and free tendon lengths. Optimal muscle fascicle lengths, pennation angles at optimal length, physiological cross-sectional areas (PCSA), and tendon slack lengths were calculated from the directly measured values. Fascicle length and pennation angle varied greatly within each subject. Average fascicle lengths normalized by optimal fascicle length varied between 0.73 and 1.25, with 75% of the formalin-preserved muscles being found in a shortened state. The muscle volume and PCSA also had a large variability within subjects but less variation between subjects. The ratio of tendon slack length to optimal fascicle length was found to vary between 1.05 and 9.56. Using this data, a deformable model of the foot can now be created. It is envisioned that deformable feet will significantly improve

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In vivo human gracilis whole muscle passive stress-sarcomere strain relationship

Journal of Experimental Biology ◽

10.1242/jeb.242722 ◽

2021 ◽

Author(s):

Lomas S. Persad ◽

Benjamin I. Binder-Markey ◽

Alexander Y. Shin ◽

Kenton R. Kaufman ◽

Richard L. Lieber

Keyword(s):

Mechanical Properties ◽

Sarcomere Length ◽

Mammalian Species ◽

Muscle Length ◽

Human Muscle ◽

Gracilis Muscle ◽

Rabbit Muscle ◽

Cross Sectional ◽

Whole Muscle

We measured the passive mechanical properties of intact, living human gracilis muscles (n=11 individuals, 1 female, age: 33±12years, mass: 89±23kg, height: 177±8cm). Measurements were performed in patients undergoing surgery for free functioning myocutaneous tissue transfer of the gracilis muscle to restore elbow flexion after brachial plexus injury. Whole muscle force of the gracilis tendon was measured in four joint configurations (JC1-JC4) with a buckle force transducer placed at the distal tendon. Sarcomere length was also measured by biopsy from the proximal gracilis muscle. After the muscle was removed a three-dimensional volumetric reconstruction of the muscle was created via photogrammetry. Muscle length from JC1 to JC4 increased by 3.3±1.0 cm, 7.7±1.2 cm, 10.5±1.3 cm and 13.4±1.2 cm respectively, corresponding to 15%, 34%, 46% and 59% muscle fiber strain respectively. Muscle volume and an average optimal fiber length of 23.1±0.7 cm yielded an average muscle physiological cross-sectional area of 6.8±0.7 cm2 which is approximately three times that measured previously from cadaveric specimens. Absolute passive tension increased from 0.90±0.21 N in JC1 to 16.50±2.64 N in JC4. As expected, sarcomere length also increased from 3.24±0.08 µm at JC1 to 3.63±0.07 µm at JC4, which are on the descending limb of the human sarcomere length-tension curve. Peak passive muscle stress was 27.8±5.5 kPa in JC4 and muscle modulus ranged from 44.8 MPa in JC1 to 125.7 MPa in JC4. Compared to other mammalian species, human muscle passive mechanical properties are more similar to rodent muscle than rabbit muscle. These data provide direct measurements of whole human muscle passive mechanical properties that can be used in modeling studies and for understanding comparative passive mechanical properties among mammalian muscles.

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