Advertisement

Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy

      Highlights

      • Shear waves travel faster in gastrocnemius of more-affected limb in hemiplegic cerebral palsy.
      • Shear wave velocity increases as torque, angle, and strain increase.
      • Muscle material properties may be altered in cerebral palsy muscle.

      Abstract

      Background

      Individuals with cerebral palsy tend to have altered muscle architecture and composition, but little is known about the muscle material properties, specifically stiffness. Shear wave ultrasound elastography allows shear wave speed, which is related to stiffness, to be measured in vivo in individual muscles. Our aim was to evaluate the material properties, specifically stiffness, as measured by shear wave speed of the medial gastrocnemius and tibialis anterior muscles in children with hemiplegic cerebral palsy across a range of ankle torques and positions, and fascicle strains.

      Method

      Shear wave speed was measured bilaterally in the medial gastrocnemius and tibialis anterior over a range of ankle positions and torques using shear wave ultrasound elastography in eight individuals with hemiplegic cerebral palsy. B-mode ultrasound was used to measure muscle thickness and fascicle strain.

      Results

      Shear waves traveled faster in the medial gastrocnemius and tibialis anterior of the more-affected limb by 14% (P = 0.024) and 20% (P = 0.03), respectively, when the ankle was at 90°. Shear wave speed in the medial gastrocnemius increased as the ankle moved from plantarflexion to dorsiflexion (less affected: r2 = 0.82, P < 0.001; more-affected: r2 = 0.69, P < 0.001) and as ankle torque increased (less affected: r2 = 0.56, P < 0.001; more-affected: r2 = 0.45, P < 0.001). In addition, shear wave speed was strongly correlated with fascicle strain (less affected: r2 = 0.63, P < 0.001; more-affected: r2 = 0.53, P < 0.001).

      Interpretation

      The higher shear wave speed in the more-affected limb of individuals with cerebral palsy indicates greater muscle stiffness, and demonstrates the clinical potential of shear wave elastography as a non-invasive tool for investigating mechanisms of altered muscle properties and informing diagnosis and treatment.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Clinical Biomechanics
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Barber L.
        • Barrett R.
        • Lichtwark G.
        Passive muscle mechanical properties of the medial gastrocnemius in young adults with spastic cerebral palsy.
        J. Biomech. 2011; 44: 2496-2500
        • Basford J.R.
        • Jenkyn T.R.
        • An K.-N.
        • Ehman R.L.
        • Heers G.
        • Kaufman K.R.
        Evaluation of healthy and diseased muscle with magnetic resonance elastography.
        Arch. Phys. Med. Rehabil. 2002; 83: 1530-1536
        • Bercoff J.
        • Tanter M.
        • Fink M.
        Supersonic shear imaging — a new technique for soft tissue elasticity mapping.
        IEEE Trans. Ultrason. Ferroelectr. Freq. Control. 2004; 51: 396-409
        • Booth C.M.
        • Cortina-Borja M.J.
        • Theologis T.N.
        Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity.
        Dev. Med. Child Neurol. 2001; 43: 314-320
        • Bouillard K.
        • Nordez A.
        • Hodges P.W.
        • Cornu C.
        • Hug F.
        Evidence of changes in load sharing during isometric elbow flexion with ramped torque.
        J. Biomech. 2012; 45: 1424-1429
        • Brandenburg J.E.
        • Eby S.F.
        • Song P.
        • Zhao H.
        • Landry B.W.
        • Kingsley-Berg S.
        • Bamlet W.R.
        • Chen S.
        • Sieck G.C.
        • An K.-N.
        Feasibility and reliability of quantifying passive muscle stiffness in young children by using shear wave ultrasound elastography.
        J. Ultrasound Med. 2015; 34: 663-670
        • Chardon M.K.
        • Suresh N.L.
        • Rymer W.Z.
        An evaluation of passive properties of spastic muscles in hemiparetic stroke survivors, Engineering in Medicine and Biology Society (EMBC).
        in: 2010 Annual International Conference of the IEEE. IEEE, 2010: 2993-2996
        • Chernak L.A.
        • DeWall R.J.
        • Lee K.S.
        • Thelen D.G.
        Length and activation dependent variations in muscle shear wave speed.
        Physiol. Meas. 2013; 34: 713-721
        • Eby S.F.
        • Song P.
        • Chen S.
        • Chen Q.
        • Greenleaf J.F.
        • An K.N.
        Validation of shear wave elastography in skeletal muscle.
        J. Biomech. 2013; 46: 2381-2387
        • Foran J.R.
        • Steinman S.
        • Barash I.
        • Chambers H.G.
        • Lieber R.L.
        Structural and mechanical alterations in spastic skeletal muscle.
        Dev. Med. Child Neurol. 2005; 47: 713-717
        • Friden J.
        • Lieber R.L.
        Spastic muscle cells are shorter and stiffer than normal cells.
        Muscle Nerve. 2003; 27: 157-164
        • Gage J.R.
        The Identification and Treatment of Gait Problems in Cerebral Palsy.
        2nd ed. Mac Keith Press, London2009
        • Gao F.
        • Zhao H.
        • Gaebler-Spira D.
        • Zhang L.-Q.
        In vivo evaluations of morphologic changes of gastrocnemius muscle fascicles and Achilles tendon in children with cerebral palsy.
        Am. J. Phys. Med. Rehabil. 2011; 90: 364-371
        • Ito J.
        • Araki A.
        • Tanaka H.
        • Tasaki T.
        • Cho K.
        • Yamazaki R.
        Muscle histopathology in spastic cerebral palsy.
        Brain Dev. 1996; 18: 299-303
        • Kwon D.P.
        • Young Gi
        • Lee Sung Uk
        • Chung Inbum
        Spastic cerebral palsy in children: dynamic sonoelastographic findings of medial gastrocnemius.
        Radiology. 2012; 263: 794-801
        • Lacourpaille L.
        • Hug F.
        • Bouillard K.
        • Hogrel J.Y.
        • Nordez A.
        Supersonic shear imaging provides a reliable measurement of resting muscle shear elastic modulus.
        Physiol. Meas. 2012; 33: N19-N28
        • Lamminen A.
        • Jääskeläinen J.
        • Rapola J.
        • Suramo I.
        High-frequency ultrasonography of skeletal muscle in children with neuromuscular disease.
        J. Ultrasound Med. 1988; 7: 505-509
        • Lee S.S.
        • Piazza S.J.
        Built for speed: musculoskeletal structure and sprinting ability.
        J. Exp. Biol. 2009; 212: 3700-3707
        • Lee S.S.
        • Spear S.
        • Rymer W.Z.
        Quantifying changes in material properties of stroke-impaired muscle.
        Clin. Biomech. 2015; 30: 269-275
        • Legerlotz K.
        • Smith H.K.
        • Hing W.A.
        Variation and reliability of ultrasonographic quantification of the architecture of the medial gastrocnemius muscle in young children.
        Clin. Physiol. Funct. Imaging. 2010; 30: 198-205
        • Lieber R.L.
        • Runesson E.
        • Einarsson F.
        • Fridén J.
        Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material.
        Muscle Nerve. 2003; 28: 464-471
        • Magid A.
        • Law D.J.
        Myofibrils bear most of the resting tension in frog skeletal muscle.
        Science. 1985; 230: 1280-1282
        • Maïsetti O.
        • Hug F.
        • Bouillard K.
        • Nordez A.
        Characterization of passive elastic properties of the human medial gastrocnemius muscle belly using supersonic shear imaging.
        J. Biomech. 2012; 45: 978-984
        • Malaiya R.
        • McNee A.E.
        • Fry N.R.
        • Eve L.C.
        • Gough M.
        • Shortland A.P.
        The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy.
        J. Electromyogr. Kinesiol. 2007; 17: 657-663
        • Marden F.A.
        • Connolly A.M.
        • Siegel M.J.
        • Rubin D.A.
        Compositional analysis of muscle in boys with Duchenne muscular dystrophy using MR imaging.
        Skelet. Radiol. 2005; 34: 140-148
        • Mathewson M.A.
        • Chambers H.G.
        • Girard P.J.
        • Tenenhaus M.
        • Schwartz A.K.
        • Lieber R.L.
        Stiff muscle fibers in calf muscles of patients with cerebral palsy lead to high passive muscle stiffness.
        J. Orthop. Res. 2014; 32: 1667-1674
        • Murphy W.A.
        • Totty W.
        • Carroll J.
        MRI of normal and pathologic skeletal muscle.
        Am. J. Roentgenol. 1986; 146: 565-574
        • Park G.-Y.
        • Kwon D.R.
        Sonoelastographic evaluation of medial gastrocnemius muscles intrinsic stiffness after rehabilitation therapy with botulinum toxin A injection in spastic cerebral palsy.
        Arch. Phys. Med. Rehabil. 2012; 93: 2085-2089
        • Pillen S.
        • Verrips A.
        • Van Alfen N.
        • Arts I.
        • Sie L.
        • Zwarts M.
        Quantitative skeletal muscle ultrasound: diagnostic value in childhood neuromuscular disease.
        Neuromuscul. Disord. 2007; 17: 509-516
        • Pillen S.
        • van Dijk J.P.
        • Weijers G.
        • Raijmann W.
        • de Korte C.L.
        • Zwarts M.J.
        Quantitative gray-scale analysis in skeletal muscle ultrasound: a comparison study of two ultrasound devices.
        Muscle Nerve. 2009; 39: 781-786
        • Ponten E.M.
        • Stal P.S.
        Decreased capillarization and a shift to fast myosin heavy chain IIx in the biceps brachii muscle from young adults with spastic paresis.
        J. Neurol. Sci. 2007; 253: 25-33
        • Prado L.G.
        • Makarenko I.
        • Andresen C.
        • Krüger M.
        • Opitz C.A.
        • Linke W.A.
        Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles.
        J. Gen. Physiol. 2005; 126: 461-480
        • Royer D.
        • Gennisson J.L.
        • Deffieux T.
        • Tanter M.
        On the elasticity of transverse isotropic soft tissues (L).
        J. Acoust. Soc. Am. 2011; 129: 2757-2760
        • Shortland A.P.
        • Harris C.A.
        • Gough M.
        • Robinson R.O.
        Architecture of the medial gastrocnemius in children with spastic diplegia.
        Dev. Med. Child Neurol. 2002; 44: 158-163
        • Sinkjær T.
        • Magnussen I.
        Passive, intrinsic and reflex-mediated stiffness in the ankle extensors of hemiparetic patients.
        Brain. 1994; 117: 355-363
        • Sinkjær T.
        • Toft E.
        • Andreassen S.
        • Hornemann B.C.
        Muscle stiffness in human ankle dorsiflexors: intrinsic and reflex components.
        J. Neurophysiol. 1988; 60: 1110-1121
        • Sinkjér T.
        • Toft E.
        • Larsen K.
        • Andreassen S.
        • Hansen H.J.
        Non-reflex and reflex mediated ankle joint stiffness in multiple sclerosis patients with spasticity.
        Muscle Nerve. 1993; 16: 69-76
        • Smith L.R.
        • Lee K.S.
        • Ward S.R.
        • Chambers H.G.
        • Lieber R.L.
        Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length.
        J. Physiol. 2011; 589: 2625-2639
        • Yeargin-Allsopp M.
        • Van Naarden Braun K.
        • Doernberg N.S.
        • Benedict R.E.
        • Kirby R.S.
        • Durkin M.S.
        Prevalence of cerebral palsy in 8-year-old children in three areas of the United States in 2002: a multisite collaboration.
        Pediatrics. 2008; 121: 547-554
        • Yoshitake Y.
        • Takai Y.
        • Kanehisa H.
        • Shinohara M.
        Muscle shear modulus measured with ultrasound shear-wave elastography across a wide range of contraction intensity.
        Muscle Nerve. 2014; 50: 103-113