Use of ultrasound shear wave to measure muscle stiffness in children with cerebral palsy

E A Vola, M Albano, C Di Luise, V Servodidio, M Sansone, S Russo, B Corrado, C Servodio Iammarrone, M G Caprio, G Vallone, E A Vola, M Albano, C Di Luise, V Servodidio, M Sansone, S Russo, B Corrado, C Servodio Iammarrone, M G Caprio, G Vallone

Abstract

Purpose: Cerebral palsy (CP) is a disorder characterized by an increased muscle stiffness that can be contingent on both neurological and biomechanical factors. The neurological aspects are related to hyper-excitability of the stretch reflex, while the biomechanical factors are related to modifications in muscle structure. We used smart-shear wave elastography (S-SWE) to analyze muscle properties and to compare shear wave speed in soleus muscles of patients affected by CP and typically developing children.

Methods: We enrolled 21 children (15 males and 6 females; age range 3-16) with spastic hemiplegia CP and 21 healthy children (11 males and 10 females; age range 3-14). Measurements of soleus S-SWE were performed using a Samsung RS80A ultrasound scanner with Prestige equipment (Samsung Medison Co. Ltd., Seoul, Korea), with a convex array transducer (CA1-7; Samsung Medison Co. Ltd., Seoul, Korea). For each CP child clinical assessment included Modified Ashworth Scale (MAS) score.

Results: Children with CP showed greater S-SWE values than the healthy ones (p < 0.001). Our data suggest a significant correlation between the S-SWE values and the MAS scores (Spearman correlation coefficient 0.74; p < 0.001 at Kruskal-Wallis test) in children with CP.

Conclusions: Measuring muscle properties with SWE, a non-invasive and real-time technique, may integrate the physical exam. SWE may be a reliable clinical tool for diagnosis and longitudinal monitoring of muscle stiffness, as well as particularly suitable for grading and for assessing the response to treatments.

Keywords: Cerebral palsy; Elastosonography; Muscle; Physiatry; Radiology; Shear wave.

Conflict of interest statement

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Human and animal rights

This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Figures

Fig. 1
Fig. 1
a Samsung S-shearwave elastography assessed on the soleus of a child with CP. The yellow box (center) represents the shear wave measurement area. The ROI depth and the RMI (reliability measurement index) are expressed below. a The elasticity measurement (11.0 kPa) is not reliable given that the RMI is equal to 0.2. b The elasticity value (7.0 kPa) is reliable since RMI measures 0.7
Fig. 2
Fig. 2
a Samsung S-shearwave elastography assessed on the soleus of a TD child. The yellow box (center) represents the shear wave measurement area. The ROI depth and the RMI (reliability measurement index) are expressed below. a The first measurement cannot be considered reliable (16.8 kPa) since RMI measures 0.0. b The second elasticity measurement (7.0 kPa) is considered reliable since RMI measures 0.5
Fig. 3
Fig. 3
Boxplot of the distributions of SWE for the two groups analyzed (CP cerebral palsy, TD typically developing). The bold line inside the box indicates the median value
Fig. 4
Fig. 4
Relationship between MAS groups and SWE. For exemplification purposes a linear regression trend has been superimposed

References

    1. Ozmen M, Caliskan M, Apak S, Gokcay G. 8 years clinical experience in cerebral palsy. J Trop Pediatr. 1993;39:52–54. doi: 10.1093/tropej/39.1.52.
    1. Lance J. Spasticity: disorders motor control. In: Feldman RG, Young RP, Koella WP, editors. Symposium synopsis. Miami, FL: Year Book Medical Publishers; 1980.
    1. Haas B, Bergstrom E, Jamous A, Bennie A. The inter rater reliability of the original and of the modified ashworth scale for the assessment of spasticity in patients with spinal cord injury. Spinal Cord. 1996;34:560–564. doi: 10.1038/sc.1996.100.
    1. Mentiplay BF, Perraton LG, Bower KJ, et al. Assessment of lower limb muscle strength and power using hand-held and fixed dynamometry: a reliability and validity study. PLoS One. 2015;10(10):e0140822. doi: 10.1371/journal.pone.0140822.
    1. Stark T, Walker B, Phillips JK, Fejer R, Beck R. Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review. PM & R. 2011;3(5):472–479. doi: 10.1016/j.pmrj.2010.10.025.
    1. Kolber MJ, Cleland JA. Strength testing using hand-held dynamometry. Phys Therapy Rev. 2005;10(2):99–112. doi: 10.1179/108331905X55730.
    1. Choi YJ, et al. Ultrasound elastography for evaluation of cervical lymph nodes. Ultrasonography. 2015;34(3):157–164. doi: 10.14366/usg.15007.
    1. Ryu J, Jeong WK. Current status of musculoskeletal application of shear wave elastography. Ultrasonography. 2017;36:185–197. doi: 10.14366/usg.16053.
    1. Klauser AS, Miyamoto H, Bellmann-Weiler R, Feuchtner GM, Wick MC, Jaschke WR. Sonoelastography: musculoskeletal applications. Radiology. 2014;272:622–633. doi: 10.1148/radiol.14121765.
    1. Drakonaki EE, Allen GM, Wilson DJ. Ultrasound elastography for musculoskeletal applications. Br J Radiol. 2012;85:1435–1445. doi: 10.1259/bjr/93042867.
    1. Kim SJ, Park HJ, Lee SY. Usefulness of strain elastography of the musculoskeletal system. Ultrasonography. 2016;35:104–109. doi: 10.14366/usg.15072.
    1. Arda K, Ciledag N, Aktas E, Aribas BK, Kose K. Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am J Roentgenol. 2011;197:532–536. doi: 10.2214/AJR.10.5449.
    1. Gennisson JL, Deffieux T, Fink M, Tanter M. Ultrasound elastography: principles and techniques. Diagn Interv Imaging. 2013;94:487–495. doi: 10.1016/j.diii.2013.01.022.
    1. Bamber J, Cosgrove D, Dietrich CF, Fromageau J, Bojunga J, Calliada F, Cantisani V, Correas JM, D’Onofrio M, Drakonaki EE, Fink M, Friedrich-Rust Gilja OH, Havre RF, Jenssen C, Klauser AS, Ohlinger R, Saftoiu A, Schaefer F, Sporea I, Piscaglia F. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall Med. 2013;34:169–184. doi: 10.1055/s-0033-1335205.
    1. Mulabecirovic A, Mjelle AB, Gilja OH, Vesterhus M, Havre RF. Repeatability of shear wave elastography in liver fibrosis phantoms—evaluation of five different systems. PLoS One. 2018;13(1):e0189671. doi: 10.1371/journal.pone.0189671.
    1. Park D-S, Kwon DR, Park G-Y, Lee MY. Therapeutic effect of extracorporeal shock wave therapy according to treatment session on gastrocnemius muscle spasticity in children with spastic cerebral palsy: a pilot study. Ann Rehabilit Med. 2015;39(6):914–921. doi: 10.5535/arm.2015.39.6.914.
    1. Prado LG, Makarenko I, Andresen C, Kruger M, Opitz CA, Linke WA. Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles. J Gen Physiol. 2005;126:461–480. doi: 10.1085/jgp.200509364.
    1. Chen X, Li Y. Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adhes Migr. 2009;3:337–341. doi: 10.4161/cam.3.4.9338.
    1. Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL. 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. doi: 10.1113/jphysiol.2010.203364.
    1. Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH, et al. EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med. 2013;34:238–253. doi: 10.1055/s-0033-1335375.
    1. Bortolotto C, Lungarotti L, Fiorina I, Zacchino M, Draghi F, Calliada F. Influence of subjects’ characteristics and technical variables on muscle stiffness measured by shear wave elastosonography. J Ultrasound. 2017;20(2):139–146. doi: 10.1007/s40477-017-0242-9.
    1. Minafra P, Bortolotto C, Rampinini E, Calliada F, Monetti G. Quantitative elastosonography of the myotendinous junction: normal behavior and correlation with a standard measurement system during functional tests. J Ultrasound Med. 2017;36(1):141–147. doi: 10.7863/ultra.15.11023.
    1. Brandenburg JE, Eby SF, Song P, Kingsley-Berg S, Bamlet W, Sieck GC, et al. Quantifying passive muscle stiffness in children with and without cerebral palsy using ultrasound shear wave elastography. Dev Med Child Neurol. 2016;58:1288–1294. doi: 10.1111/dmcn.13179.
    1. Lee SS, Gaebler-Spira D, Zhang LQ, Rymer WZ, Steele KM. Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy. Clin Biomech. 2016;31:20–28. doi: 10.1016/j.clinbiomech.2015.10.006.
    1. Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN. Validation of shear wave elastography in skeletal muscle. J Biomech. 2013;46(14):2381–2387. doi: 10.1016/j.jbiomech.2013.07.033.

Source: PubMed

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