Ultrasound as a Tool to Study Muscle–Tendon Functions during Locomotion: A Systematic Review of Applications

Movement science investigating muscle and tendon functions during locomotion utilizes commercial ultrasound imagers built for medical applications. These limit biomechanics research due to their form factor, range of view, and spatio-temporal resolution. This review systematically investigates the technical aspects of applying ultrasound as a research tool to investigate human and animal locomotion. It provides an overview on the ultrasound systems used and of their operating parameters. We present measured fascicle velocities and discuss the results with respect to operating frame rates during recording. Furthermore, we derive why muscle and tendon functions should be recorded with a frame rate of at least 150 Hz and a range of view of 250 mm. Moreover, we analyze why and how the development of better ultrasound observation devices at the hierarchical level of muscles and tendons can support biomechanics research. Additionally, we present recent technological advances and their possible application. We provide a list of recommendations for the development of a more advanced ultrasound sensor system class targeting biomechanical applications. Looking to the future, mobile, ultrafast ultrasound hardware technologies create immense opportunities to expand the existing knowledge of human and animal movement.

[1]  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.

[2]  Sigrid Thaller,et al.  Determination of individual knee-extensor properties from leg extensions and parameter identification , 2017 .

[3]  Neil J Cronin,et al.  The use of ultrasound to study muscle-tendon function in human posture and locomotion. , 2013, Gait & posture.

[4]  Tim W Dorn,et al.  Muscular strategy shift in human running: dependence of running speed on hip and ankle muscle performance , 2012, Journal of Experimental Biology.

[5]  Pascal Alexander Hager.  Design of Fully-Digital Medical Ultrasound Imaging Systems , 2019 .

[6]  Thomas Deffieux,et al.  Ultrafast imaging of in vivo muscle contraction using ultrasound , 2006 .

[7]  Glen A. Lichtwark,et al.  Ultrasound technology for examining the mechanics of the muscle, tendon, and ligament , 2017 .

[8]  Takahito Suzuki,et al.  Forefoot running requires shorter gastrocnemius fascicle length than rearfoot running , 2019, Journal of sports sciences.

[9]  Neil J Cronin,et al.  Mechanical and neural function of triceps surae in elite racewalking. , 2016, Journal of applied physiology.

[10]  M. Fink,et al.  Ultrafast compound imaging for 2-D motion vector estimation: application to transient elastography , 2002, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

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

[12]  Jayishni N. Maharaj,et al.  The mechanical function of the tibialis posterior muscle and its tendon during locomotion. , 2016, Journal of biomechanics.

[13]  Rodger Kram,et al.  Muscle contributions to propulsion and braking during walking and running: insight from external force perturbations. , 2014, Gait & posture.

[14]  F.E. Zajac,et al.  An interactive graphics-based model of the lower extremity to study orthopaedic surgical procedures , 1990, IEEE Transactions on Biomedical Engineering.

[15]  Jørgen Arendt Jensen,et al.  Synthetic aperture ultrasound imaging. , 2006, Ultrasonics.

[16]  Ajay Seth,et al.  Muscle contributions to propulsion and support during running. , 2010, Journal of biomechanics.

[17]  Scott L. Delp,et al.  A Model of the Lower Limb for Analysis of Human Movement , 2010, Annals of Biomedical Engineering.

[18]  M. Fink,et al.  Ultrafast imaging of the heart using circular wave synthetic imaging with phased arrays , 2009, 2009 IEEE International Ultrasonics Symposium.

[19]  W. Herzog,et al.  Force enhancement following stretching of skeletal muscle: a new mechanism. , 2002, The Journal of experimental biology.

[20]  Benedicte Vanwanseele,et al.  Effect of habitual foot-strike pattern on the gastrocnemius medialis muscle-tendon interaction and muscle force production during running. , 2019, Journal of applied physiology.

[21]  Piero Tortoli,et al.  A real-time beamformer for high frame rate ultrasound imaging , 2016, 2016 IEEE International Ultrasonics Symposium (IUS).

[22]  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.

[23]  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.

[24]  D. Farris,et al.  Human medial gastrocnemius force–velocity behavior shifts with locomotion speed and gait , 2012, Proceedings of the National Academy of Sciences.

[25]  M. Pandy,et al.  In vivo behavior of the human soleus muscle with increasing walking and running speeds. , 2015, Journal of applied physiology.

[26]  L. Nuri,et al.  Regional three‐dimensional deformation of human Achilles tendon during conditioning , 2017, Scandinavian journal of medicine & science in sports.

[27]  P. Komi.  Stretch-shortening cycle: a powerful model to study normal and fatigued muscle. , 2000, Journal of biomechanics.

[28]  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.

[29]  A. Arndt,et al.  Ultrasound-based testing of tendon mechanical properties: a critical evaluation. , 2015, Journal of applied physiology.

[30]  Ayman Habib,et al.  OpenSim: Simulating musculoskeletal dynamics and neuromuscular control to study human and animal movement , 2018, PLoS Comput. Biol..

[31]  G. Lichtwark,et al.  Muscle-tendon length and force affect human tibialis anterior central aponeurosis stiffness in vivo , 2018, Proceedings of the National Academy of Sciences.

[32]  Luca Modenese,et al.  Medial gastrocnemius and soleus muscle‐tendon unit, fascicle, and tendon interaction during walking in children with cerebral palsy , 2017, Developmental medicine and child neurology.

[33]  D. Grieve.  Prediction of gastrocnemius length from knee and ankle joint posture , 1978 .

[34]  S. I. Nikolov,et al.  SARUS: A synthetic aperture real-time ultrasound system , 2013, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[35]  O. Schmitt.  The heat of shortening and the dynamic constants of muscle , 2017 .

[36]  A. Huxley,et al.  The variation in isometric tension with sarcomere length in vertebrate muscle fibres , 1966, The Journal of physiology.

[37]  R. F. Ker,et al.  The role of tendon elasticity in the locomotion of the camel (Camelus dromedarius) , 2009 .

[38]  R. Alexander,et al.  Storage of elastic strain energy in muscle and other tissues , 1977, Nature.

[39]  Paavo V. Komi,et al.  Can measures of muscle–tendon interaction improve our understanding of the superiority of Kenyan endurance runners? , 2014, European Journal of Applied Physiology.

[40]  E. Konofagou,et al.  A composite high-frame-rate system for clinical cardiovascular imaging , 2008, IEEE Transactions on Ultrasonics, Ferroelectrics and Frequency Control.

[41]  Mickael Tanter,et al.  Ultrafast imaging in biomedical ultrasound , 2014, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[42]  D. Moher,et al.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. , 2010, International journal of surgery.

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

[44]  R. F. Ker,et al.  Elastic extension of leg tendons in the locomotion of horses (Equus caballus) , 2009 .

[45]  Min-Ho Song,et al.  How Fast Is Your Body Motion? Determining a Sufficient Frame Rate for an Optical Motion Tracking System Using Passive Markers , 2016, PloS one.

[46]  W S Levine,et al.  An optimal control model for maximum-height human jumping. , 1990, Journal of biomechanics.

[47]  M G Pandy,et al.  Differences in in vivo muscle fascicle and tendinous tissue behavior between the ankle plantarflexors during running , 2018, Scandinavian journal of medicine & science in sports.

[48]  Marcus G Pandy,et al.  Muscle and joint function in human locomotion. , 2010, Annual review of biomedical engineering.

[49]  R. M. Alexander.  Energy-saving mechanisms in walking and running. , 1991, The Journal of experimental biology.

[50]  Piero Tortoli,et al.  ULA-OP 256: A 256-Channel Open Scanner for Development and Real-Time Implementation of New Ultrasound Methods , 2016, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[51]  P. Komi,et al.  Age‐specific neuromuscular interaction during elderly habitual running , 2015, Acta physiologica.

[52]  B. C. Abbott,et al.  MUSCLE MECHANICS. , 1963, Revue canadienne de biologie.

[53]  Samuel R. Hamner,et al.  Muscle contributions to fore-aft and vertical body mass center accelerations over a range of running speeds. , 2013, Journal of biomechanics.

[54]  Alexander Rm,et al.  Energy-saving mechanisms in walking and running. , 1991 .

[55]  T. Barbosa,et al.  The effects of backpack carriage on gait kinematics and kinetics of schoolchildren , 2019, Scientific Reports.

[56]  Neil J Cronin,et al.  Treadmill versus overground and barefoot versus shod comparisons of triceps surae fascicle behaviour in human walking and running. , 2013, Gait & posture.

[57]  T P Andriacchi,et al.  Studies of human locomotion: past, present and future. , 2000, Journal of biomechanics.

[58]  Stephen J Piazza,et al.  Determination of subtalar joint axis location by restriction of talocrural joint motion. , 2007, Gait & posture.

[59]  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.

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

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

[62]  Luca Benini,et al.  LightProbe: A 64-channel programmable ultrasound transducer head with an integrated front-end and a 26.4 Gb/s optical link , 2017, 2017 IEEE International Symposium on Circuits and Systems (ISCAS).

[63]  Mickael Tanter,et al.  High-contrast ultrafast imaging of the heart , 2014, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[64]  Luca Benini,et al.  Wireless sensor networks: Enabling technology for ambient intelligence , 2006, Microelectron. J..

[65]  A Arampatzis,et al.  Operating length and velocity of human vastus lateralis muscle during walking and running , 2018, Scientific Reports.

[66]  Luca Benini,et al.  UltraLight: An ultrafast imaging platform based on a digital 64-channel ultrasound probe , 2017, 2017 IEEE International Ultrasonics Symposium (IUS).

[67]  Harald Penasso,et al.  Model-based analysis of fatigued human knee extensors , 2018, European Journal of Applied Physiology.

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

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

[70]  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.

[71]  Piero Tortoli,et al.  Ultrasound Open Platforms for Next-Generation Imaging Technique Development , 2018, IEEE Transactions on Ultrasonics, Ferroelectrics, and Frequency Control.

[72]  Walter Herzog,et al.  The mysteries of eccentric muscle action , 2018, Journal of sport and health science.

[73]  T J Roberts,et al.  Muscular Force in Running Turkeys: The Economy of Minimizing Work , 1997, Science.