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.
Sommario
Obiettivo
La paralisi cerebrale infantile (PCI) è un disturbo caratterizzato da un aumento del tono muscolare che dipende da fattori sia neurologici che biomeccanici. I primi comprendono un’aumentata eccitabilità del riflesso di stiramento; la componente biomeccanica è correlata a modifiche nella struttura muscolare. Abbiamo usato l’elastosonografia con tecnologia Smart-Shear Wave (S-SWE) per analizzare le proprietà del muscolo e per comparare la velocità dell’onda di taglio nei muscoli solei di pazienti affetti da PCI con quella misurata nei soggetti sani.
Metodi
Sono stati arruolati 21 bambini (15 maschi e 6 femmine; range di età 3–16 anni) con emiplegia spastica da esiti di PCI e 21 bambini sani (11 maschi e 10 femmine; range di età 3–14 anni). Le misurazioni S-SWE del soleo sono state effettuate usando un ecografo RS80 with Prestige (Samsung Medison Co. Ltd., Seoul, Korea), con una sonda convex (CA1-7; Samsung Medison Co. Ltd., Seoul, Korea). Per ogni paziente affetto da PCI è stato valutato anche il punteggio della Modified Ashworth Scale (MAS).
Risultati
I bambini affetti da PCI hanno mostrato valori di S-SWE più alti rispetto ai controlli sani (p < 0.001). I nostri dati suggeriscono una correlazione significativa tra i valori di S-SWE e i punteggi della MAS nei pazienti affetti da PCI (coefficiente di correlazione di Spearman 0.74; p < 0.001 al Kruskal–Wallis test).
Conclusioni
La misurazione delle proprietà elastiche dei muscoli mediante S-SWE, una metodica real-time e non invasiva, può integrare l’esame clinico. La S-SWE può essere uno strumento clinico affidabile per la diagnosi e per il follow-up della stiffness muscolare, particolarmente adatto per definirne il grado e per valutarne la risposta ad un trattamento.
Similar content being viewed by others
References
Ozmen M, Caliskan M, Apak S, Gokcay G (1993) 8 years clinical experience in cerebral palsy. J Trop Pediatr 39:52–54. https://doi.org/10.1093/tropej/39.1.52
Lance J (1980) Spasticity: disorders motor control. In: Feldman RG, Young RP, Koella WP (eds) Symposium synopsis. Year Book Medical Publishers, Miami, FL
Haas B, Bergstrom E, Jamous A, Bennie A (1996) 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 34:560–564. https://doi.org/10.1038/sc.1996.100
Mentiplay BF, Perraton LG, Bower KJ et al (2015) Assessment of lower limb muscle strength and power using hand-held and fixed dynamometry: a reliability and validity study. PLoS One 10(10):e0140822
Stark T, Walker B, Phillips JK, Fejer R, Beck R (2011) Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review. PM & R 3(5):472–479
Kolber MJ, Cleland JA (2005) Strength testing using hand-held dynamometry. Phys Therapy Rev 10(2):99–112
Choi YJ et al (2015) Ultrasound elastography for evaluation of cervical lymph nodes. Ultrasonography 34(3):157–164
Ryu J, Jeong WK (2017) Current status of musculoskeletal application of shear wave elastography. Ultrasonography 36:185–197
Klauser AS, Miyamoto H, Bellmann-Weiler R, Feuchtner GM, Wick MC, Jaschke WR (2014) Sonoelastography: musculoskeletal applications. Radiology 272:622–633
Drakonaki EE, Allen GM, Wilson DJ (2012) Ultrasound elastography for musculoskeletal applications. Br J Radiol 85:1435–1445
Kim SJ, Park HJ, Lee SY (2016) Usefulness of strain elastography of the musculoskeletal system. Ultrasonography 35:104–109
Arda K, Ciledag N, Aktas E, Aribas BK, Kose K (2011) Quantitative assessment of normal soft-tissue elasticity using shear-wave ultrasound elastography. AJR Am J Roentgenol 197:532–536
Gennisson JL, Deffieux T, Fink M, Tanter M (2013) Ultrasound elastography: principles and techniques. Diagn Interv Imaging 94:487–495
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 (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 1: Basic principles and technology. Ultraschall Med 34:169–184
Mulabecirovic A, Mjelle AB, Gilja OH, Vesterhus M, Havre RF (2018) Repeatability of shear wave elastography in liver fibrosis phantoms—evaluation of five different systems. PLoS One 13(1):e0189671. https://doi.org/10.1371/journal.pone.0189671
Park D-S, Kwon DR, Park G-Y, Lee MY (2015) 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 39(6):914–921
Prado LG, Makarenko I, Andresen C, Kruger M, Opitz CA, Linke WA (2005) Isoform diversity of giant proteins in relation to passive and active contractile properties of rabbit skeletal muscles. J Gen Physiol 126:461–480
Chen X, Li Y (2009) Role of matrix metalloproteinases in skeletal muscle: migration, differentiation, regeneration and fibrosis. Cell Adhes Migr 3:337–341
Smith LR, Lee KS, Ward SR, Chambers HG, Lieber RL (2011) Hamstring contractures in children with spastic cerebral palsy result from a stiffer extracellular matrix and increased in vivo sarcomere length. J Physiol 589:2625–2639
Cosgrove D, Piscaglia F, Bamber J, Bojunga J, Correas JM, Gilja OH et al (2013) EFSUMB guidelines and recommendations on the clinical use of ultrasound elastography. Part 2: Clinical applications. Ultraschall Med 34:238–253
Bortolotto C, Lungarotti L, Fiorina I, Zacchino M, Draghi F, Calliada F (2017) Influence of subjects’ characteristics and technical variables on muscle stiffness measured by shear wave elastosonography. J Ultrasound 20(2):139–146
Minafra P, Bortolotto C, Rampinini E, Calliada F, Monetti G (2017) Quantitative elastosonography of the myotendinous junction: normal behavior and correlation with a standard measurement system during functional tests. J Ultrasound Med 36(1):141–147
Brandenburg JE, Eby SF, Song P, Kingsley-Berg S, Bamlet W, Sieck GC et al (2016) Quantifying passive muscle stiffness in children with and without cerebral palsy using ultrasound shear wave elastography. Dev Med Child Neurol 58:1288–1294. https://doi.org/10.1111/dmcn.13179
Lee SS, Gaebler-Spira D, Zhang LQ, Rymer WZ, Steele KM (2016) Use of shear wave ultrasound elastography to quantify muscle properties in cerebral palsy. Clin Biomech 31:20–28. https://doi.org/10.1016/j.clinbiomech.2015.10.006
Eby SF, Song P, Chen S, Chen Q, Greenleaf JF, An KN (2013) Validation of shear wave elastography in skeletal muscle. J Biomech 46(14):2381–2387
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Rights and permissions
About this article
Cite this article
Vola, E.A., Albano, M., Di Luise, C. et al. Use of ultrasound shear wave to measure muscle stiffness in children with cerebral palsy. J Ultrasound 21, 241–247 (2018). https://doi.org/10.1007/s40477-018-0313-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40477-018-0313-6