The use of ultrasound to study muscle-tendon function in human posture and locomotion.

Analysis of human movement has traditionally relied on measures such as kinematics, kinetics and electromyography. These measures provide valuable information about movement performance and make it possible to draw inferences about muscle and tendon function. Musculoskeletal models are also used frequently to examine the relationship between joint kinematics and muscle-tendon behaviour, and have provided important insights into both healthy and clinical gait. However, muscles interact with compliant tendons during movement, which complicates interpretation of muscle and tendon function based on external measures such as joint kinematics. Accordingly, methods have been developed that enable muscle and tendinous tissues to be imaged in real-time. Ultrasound is among the most popular methods used for this purpose, and has been applied extensively to the study of in vivo muscle and tendon function in a range of human populations and movement contexts. There is a growing body of literature that proposes different measures of muscle and/or tendon function, and these results need to be discussed in light of the technical differences between the measurement techniques. In this review we first outline the various uses of ultrasound to examine human muscle and tendon function, and then summarise ultrasound-based research specifically during locomotion and postural conditions. We then describe some of the many technical issues associated with this method. Methods of data analysis are introduced, including novel automated techniques that improve the efficiency of the analysis process. Finally, possible future directions in musculoskeletal ultrasound research are discussed.

[1]  Ayman Habib,et al.  OpenSim: Open-Source Software to Create and Analyze Dynamic Simulations of Movement , 2007, IEEE Transactions on Biomedical Engineering.

[2]  Michael Voigt,et al.  Effects of prolonged walking on neural and mechanical components of stretch responses in the human soleus muscle , 2009, The Journal of physiology.

[3]  S. Gandevia,et al.  In vivo passive mechanical behaviour of muscle fascicles and tendons in human gastrocnemius muscle–tendon units , 2011, The Journal of physiology.

[4]  Li-Qun Zhang,et al.  Ultrasonic evaluations of Achilles tendon mechanical properties poststroke. , 2009, Journal of applied physiology.

[5]  C. Maganaris Tendon conditioning: artefact or property? , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  Neil J Cronin,et al.  Automatic tracking of medial gastrocnemius fascicle length during human locomotion. , 2011, Journal of applied physiology.

[7]  T. Fukunaga,et al.  In vivo behaviour of human muscle tendon during walking , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  Takashi Komeda,et al.  Automatic detection method of muscle fiber movement as revealed by ultrasound images. , 2009, Medical engineering & physics.

[9]  V Reggie Edgerton,et al.  In vivo intramuscular fascicle-aponeuroses dynamics of the human medial gastrocnemius during plantarflexion and dorsiflexion of the foot. , 2009, Journal of applied physiology.

[10]  J H van Dieën,et al.  Lower-limb biomechanics during stair descent: influence of step-height and body mass , 2008, Journal of Experimental Biology.

[11]  Jim Dowling,et al.  The effect of ultrasound probe orientation on muscle architecture measurement. , 2007, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[12]  T. Roberts,et al.  Biaxial strain and variable stiffness in aponeuroses , 2009, The Journal of physiology.

[13]  C. Saltzman,et al.  Foot and Ankle International. , 2013, Foot & ankle international.

[14]  Constantinos N Maganaris,et al.  Active, non‐spring‐like muscle movements in human postural sway: how might paradoxical changes in muscle length be produced? , 2005, The Journal of physiology.

[15]  Jaap Harlaar,et al.  Effects of growth on geometry of gastrocnemius muscle in children: a three‐dimensional ultrasound analysis , 2011, Journal of anatomy.

[16]  P. Komi,et al.  Muscle-tendon interaction and elastic energy usage in human walking. , 2005, Journal of applied physiology.

[17]  P. Cerretelli,et al.  In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. , 1996, The Journal of physiology.

[18]  Michael Voigt,et al.  Mechanical and neural stretch responses of the human soleus muscle at different walking speeds , 2009, The Journal of physiology.

[19]  P V Komi,et al.  The role of the stretch reflex in the gastrocnemius muscle during human locomotion at various speeds. , 2007, Journal of applied physiology.

[20]  Peter A Huijing,et al.  Anatomical information is needed in ultrasound imaging of muscle to avoid potentially substantial errors in measurement of muscle geometry , 2009, Muscle & nerve.

[21]  C. Maganaris,et al.  Ageing of human muscles and tendons , 2008, Disability and rehabilitation.

[22]  M. Narici,et al.  Behavior of human muscle fascicles during shortening and lengthening contractions in vivo. , 2003, Journal of applied physiology.

[23]  Heng Zhao,et al.  Automatic tracking of muscle fascicles in ultrasound images using localized radon transform , 2011, IEEE Transactions on Biomedical Engineering.

[24]  Achilles tendon length changes during walking in long-term diabetes patients. , 2010, Clinical biomechanics.

[25]  S. Gandevia,et al.  Change in length of relaxed muscle fascicles and tendons with knee and ankle movement in humans , 2002, The Journal of physiology.

[26]  T. Fukunaga,et al.  Ultrasonography gives directly but noninvasively elastic characteristic of human tendon in vivo , 1995, European Journal of Applied Physiology and Occupational Physiology.

[27]  Gary S Chleboun,et al.  Fascicle length change of the human tibialis anterior and vastus lateralis during walking. , 2007, The Journal of orthopaedic and sports physical therapy.

[28]  James M. Wakeling,et al.  Motor unit recruitment for dynamic tasks: current understanding and future directions , 2008, Journal of Comparative Physiology B.

[29]  Rod Barrett,et al.  Validation of a freehand 3D ultrasound system for morphological measures of the medial gastrocnemius muscle. , 2009, Journal of biomechanics.

[30]  J P Paul,et al.  Load-elongation characteristics of in vivo human tendon and aponeurosis. , 2000, The Journal of experimental biology.

[31]  T. Fukunaga,et al.  Longitudinal and transverse deformation of human Achilles tendon induced by isometric plantar flexion at different intensities. , 2011, Journal of applied physiology.

[32]  Ian David Loram,et al.  Use of ultrasound to make noninvasive in vivo measurement of continuous changes in human muscle contractile length. , 2006, Journal of applied physiology.

[33]  Adamantios Arampatzis,et al.  Reproducibility of gastrocnemius medialis muscle architecture during treadmill running. , 2011, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[34]  S. Delp,et al.  Hamstrings and psoas lengths during normal and crouch gait: Implications for muscle‐tendon surgery , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[35]  T Fukunaga,et al.  Tendinous movement of a human muscle during voluntary contractions determined by real-time ultrasonography. , 1996, Journal of applied physiology.

[36]  T Fukunaga,et al.  Nonisometric behavior of fascicles during isometric contractions of a human muscle. , 1998, Journal of applied physiology.

[37]  T. Fukunaga,et al.  In vivo Mechanical Properties of Proximal and Distal Aponeuroses in Human Tibialis Anterior Muscle , 2001, Cells Tissues Organs.

[38]  L. Ardigò,et al.  Gastrocnemius muscle–tendon behaviour during walking in young and older adults , 2007, Acta physiologica.

[39]  K. Roeleveld,et al.  Inhomogeneities in muscle activation reveal motor unit recruitment. , 2005, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[40]  M. Pinzur,et al.  Achilles Tendinopathy in Diabetes Mellitus , 2008 .

[41]  D. Thelen,et al.  Measurement of tendon strain during muscle twitch contractions using ultrasound elastography , 2009, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[42]  M. Hull,et al.  A method for determining lower extremity muscle-tendon lengths during flexion/extension movements. , 1990, Journal of biomechanics.

[43]  G. A. Lichtwarka,et al.  Optimal muscle fascicle length and tendon stiffness for maximising gastrocnemius efficiency during human walking and running , 2008 .

[44]  Jason C Gillette,et al.  Lower extremity mechanics of iliotibial band syndrome during an exhaustive run. , 2007, Gait & posture.

[45]  Adamantios Arampatzis,et al.  Reproducibility of fascicle length and pennation angle of gastrocnemius medialis in human gait in vivo. , 2010, Gait & posture.

[46]  G. Lichtwark,et al.  Muscle fascicle and series elastic element length changes along the length of the human gastrocnemius during walking and running. , 2007, Journal of biomechanics.

[47]  A. Blazevich,et al.  In vivo assessment of muscle fascicle length by extended field-of-view ultrasonography. , 2010, Journal of applied physiology.

[48]  Thomas Stretch Dowse,et al.  MUSCLE AND NERVE , 1903 .

[49]  James M Wakeling,et al.  In-vivo determination of 3D muscle architecture of human muscle using free hand ultrasound. , 2011, Journal of biomechanics.

[50]  C. Maganaris,et al.  In vivo measurements of the triceps surae complex architecture in man: implications for muscle function , 1998, The Journal of physiology.

[51]  P. Aagaard,et al.  Mechanical properties of the human Achilles tendon, in vivo. , 2011, Clinical biomechanics.

[52]  M. Kjaer,et al.  Differential displacement of the human soleus and medial gastrocnemius aponeuroses during isometric plantar flexor contractions in vivo. , 2004, Journal of applied physiology.

[53]  Ghassan Hamarneh,et al.  Automated Tracking of Muscle Fascicle Orientation in B-mode Ultrasound Images , 2022 .

[54]  D. Stegeman,et al.  Dynamic imaging of skeletal muscle contraction in three orthogonal directions. , 2010, Journal of applied physiology.

[55]  S. Riek,et al.  Recruitment of motor units in human forearm extensors. , 1992, Journal of neurophysiology.

[56]  Vasilios Baltzopoulos,et al.  Predictability of in vivo changes in pennation angle of human tibialis anterior muscle from rest to maximum isometric dorsiflexion , 1999, European Journal of Applied Physiology and Occupational Physiology.

[57]  M Gough,et al.  Three-dimensional realisation of muscle morphology and architecture using ultrasound. , 2004, Gait & posture.

[58]  G. Lichtwark,et al.  In vivo mechanical properties of the human Achilles tendon during one-legged hopping , 2005, Journal of Experimental Biology.

[59]  Constantinos N Maganaris,et al.  Paradoxical muscle movement in human standing , 2004, The Journal of physiology.

[60]  T. Finni,et al.  Intermuscular force transmission between human plantarflexor muscles in vivo. , 2010, Journal of applied physiology.

[61]  T Sinkjaer,et al.  Afferent contribution to locomotor muscle activity during unconstrained overground human walking: an analysis of triceps surae muscle fascicles. , 2010, Journal of neurophysiology.

[62]  Tommy Löfstedt,et al.  Modelling human musculoskeletal functional movements using ultrasound imaging , 2010, BMC Medical Imaging.

[63]  T. Fukunaga,et al.  Architectural and functional features of human triceps surae muscles during contraction. , 1998, Journal of applied physiology.

[64]  P V Komi,et al.  Medial gastrocnemius muscle behavior during human running and walking. , 2007, Gait & posture.

[65]  D L Benoit,et al.  Muscle activation and length changes during two lunge exercises: implications for rehabilitation , 2009, Scandinavian journal of medicine & science in sports.

[66]  P. Huijing Muscular Force Transmission Necessitates a Multilevel Integrative Approach to the Analysis of Function of Skeletal Muscle , 2003, Exercise and sport sciences reviews.

[67]  François Hug,et al.  Estimation of Individual Muscle Force Using Elastography , 2011, PloS one.

[68]  M. Kjaer,et al.  Differential strain patterns of the human gastrocnemius aponeurosis and free tendon, in vivo. , 2003, Acta physiologica Scandinavica.

[69]  G. Lichtwark,et al.  Interactions between the human gastrocnemius muscle and the Achilles tendon during incline, level and decline locomotion , 2006, Journal of Experimental Biology.

[70]  T Fukunaga,et al.  Influence of elastic properties of tendon structures on jump performance in humans. , 1999, Journal of applied physiology.

[71]  J. P. Paul,et al.  In vivo human tendon mechanical properties , 1999, The Journal of physiology.

[72]  P. Komi,et al.  Individual muscle contributions to the in vivo achilles tendon force. , 1998, Clinical biomechanics.

[73]  J. P. Paul,et al.  In vivo human tendinous tissue stretch upon maximum muscle force generation. , 2000, Journal of biomechanics.

[74]  J. Avela,et al.  In vivo mechanical response of human Achilles tendon to a single bout of hopping exercise , 2010, Journal of Experimental Biology.

[75]  V. Edgerton,et al.  Nonuniform strain of human soleus aponeurosis-tendon complex during submaximal voluntary contractions in vivo. , 2003, Journal of applied physiology.

[76]  P V Komi,et al.  Interaction between fascicle and tendinous tissues in short-contact stretch-shortening cycle exercise with varying eccentric intensities. , 2005, Journal of applied physiology.

[77]  J H van Dieën,et al.  Influence of step-height and body mass on gastrocnemius muscle fascicle behavior during stair ascent. , 2008, Journal of biomechanics.

[78]  Yasuo Kawakami,et al.  In vivo determination of fascicle curvature in contracting human skeletal muscles. , 2002, Journal of applied physiology.

[79]  Zhaohua Ding,et al.  Combined diffusion and strain tensor MRI reveals a heterogeneous, planar pattern of strain development during isometric muscle contraction. , 2011, American journal of physiology. Regulatory, integrative and comparative physiology.

[80]  Johan G Bosch,et al.  Development and validation of ultrasound speckle tracking to quantify tendon displacement. , 2010, Journal of biomechanics.

[81]  Jarred G Gillett,et al.  Reliability and accuracy of an automated tracking algorithm to measure controlled passive and active muscle fascicle length changes from ultrasound , 2013, Computer methods in biomechanics and biomedical engineering.