Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

Quantitative Evaluation of Gastrocnemius Medialis Stiffness During Passive Stretching Using Shear Wave Elastography in Patients with Parkinson's Disease: A Prospective Preliminary Study

  • Lu Yin (Department of Ultrasound, Beijing Tiantan Hospital, Capital Medical University) ;
  • Lijuan Du (Department of Ultrasound, Beijing Tiantan Hospital, Capital Medical University) ;
  • Yuanzi Li (Department of Ultrasound, Beijing Tiantan Hospital, Capital Medical University) ;
  • Yang Xiao (Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences) ;
  • Shiquan Zhang (Institute of Biomedical and Health Engineering, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences) ;
  • Huizi Ma (Center for Movement Disorders, Department of Neurology, Beijing Tiantan Hospital, Capital Medical University) ;
  • Wen He (Department of Ultrasound, Beijing Tiantan Hospital, Capital Medical University)
  • Received : 2020.06.27
  • Accepted : 2021.06.01
  • Published : 2021.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: To prospectively investigate the feasibility of shear wave elastography (SWE) as a new quantitative and objective method for evaluating the stiffness of the gastrocnemius medialis (GM) muscle during passive stretching in patients with Parkinson's disease (PD). Materials and Methods: SWE of the GM muscle was performed in 28 patients with PD [13 female and 15 male; mean age ± standard deviation (SD): 63.0 ± 8.5 years] and 12 healthy controls (5 female and 7 male; mean age ± SD: 59.3 ± 6.4 years) during passive ankle rotation. A Young's modulus-ankle angle curve was constructed. The GM slack angle and baseline Young's modulus (E0) were compared between the markedly symptomatic and mildly symptomatic sides of patients with PD, and healthy controls. Additionally, the correlation between the GM slack angle and the severity of rigidity, and the observer reproducibility of SWE in determining the GM slack angle were evaluated. Results: The GM slack angle was smaller on both the markedly and mildly symptomatic sides in patients with PD than in healthy controls (mean ± SD of -29.13° ± 3.79° and -25.65° ± 3.39°, respectively, vs. -21.22° ± 3.52°; p < 0.001 and p = 0.006, respectively). Additionally, in patients with PD, the GM slack angle on the markedly symptomatic side was smaller than that on the mildly symptomatic side (p = 0.003). The E0 value was lower on both the markedly and mildly symptomatic sides in patients with PD than in healthy controls (mean ± SD of 10.11 ± 2.85 kPa and 10.08 ± 1.88 kPa, respectively, vs. 12.23 ± 1.02 kPa; p = 0.012 and p < 0.001, respectively). However, no significant difference was found between the markedly and mildly symptomatic sides in patients with PD (p = 0.634). A negative linear relationship was observed between the GM slack angle and lower limb rigidity score on the markedly symptomatic side in patients with PD (r = -0.719; p < 0.001). The intraclass correlation coefficients for observer reproducibility of SWE ranged from 0.880 to 0.951. Conclusion: The slack angle determined by SWE may be a useful quantitative and reproducible method for evaluating muscle stiffness in patients with PD.

Keywords

Acknowledgement

We gratefully thank all participants for their collaboration in this study.

References

  1. Jankovic J. Parkinson's disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry 2008;79:368-376
  2. Ascherio A, Schwarzschild MA. The epidemiology of Parkinson's disease: risk factors and prevention. Lancet Neurol 2016;15:1257-1272
  3. Berardelli A, Sabra AF, Hallett M. Physiological mechanisms of rigidity in Parkinson's disease. J Neurol Neurosurg Psychiatry 1983;46:45-53
  4. Gajdosik RL. Passive extensibility of skeletal muscle: review of the literature with clinical implications. Clin Biomech (Bristol, Avon) 2001;16:87-101
  5. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967;17:427-442
  6. Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 2008;23:2129-2170
  7. Rizzo G, Copetti M, Arcuti S, Martino D, Fontana A, Logroscino G. Accuracy of clinical diagnosis of Parkinson disease: a systematic review and meta-analysis. Neurology 2016;86:566-576
  8. Marusiak J, Jaskolska A, Budrewicz S, Koszewicz M, Jaskolski A. Increased muscle belly and tendon stiffness in patients with Parkinson's disease, as measured by myotonometry. Mov Disord 2011;26:2119-2122
  9. Creze M, Soubeyrand M, Yue JL, Gagey O, Maitre X, Bellin MF. Magnetic resonance elastography of the lumbar back muscles: a preliminary study. Clin Anat 2018;31:514-520
  10. Wang CK, Fang YD, Lin LC, Lin CF, Kuo LC, Chiu FM, et al. Magnetic resonance elastography in the assessment of acute effects of kinesio taping on lumbar paraspinal muscles. J Magn Reson Imaging 2019;49:1039-1045
  11. Gao J, He W, Du LJ, Li S, Cheng LG, Shih G, et al. Ultrasound strain elastography in assessment of resting biceps brachii muscle stiffness in patients with Parkinson's disease: a primary observation. Clin Imaging 2016;40:440-444
  12. Klauser AS, Miyamoto H, Bellmann-Weiler R, Feuchtner GM, Wick MC, Jaschke WR. Sonoelastography: musculoskeletal applications. Radiology 2014;272:622-633
  13. Liu J, Ji Y, Ai H, Ning B, Zhao J, Zhang Y, et al. Liver shear-wave velocity and serum fibrosis markers to diagnose hepatic fibrosis in patients with chronic viral hepatitis B. Korean J Radiol 2016;17:396-404
  14. Bensamoun SF, Wang L, Robert L, Charleux F, Latrive JP, Ho Ba Tho MC. Measurement of liver stiffness with two imaging techniques: magnetic resonance elastography and ultrasound elastometry. J Magn Reson Imaging 2008;28:1287-1292
  15. Yoon JH, Lee JM, Woo HS, Yu MH, Joo I, Lee ES, et al. Staging of hepatic fibrosis: comparison of magnetic resonance elastography and shear wave elastography in the same individuals. Korean J Radiol 2013;14:202-212
  16. Oudry J, Chen J, Glaser KJ, Miette V, Sandrin L, Ehman RL. Cross-validation of magnetic resonance elastography and ultrasound-based transient elastography: a preliminary phantom study. J Magn Reson Imaging 2009;30:1145-1150
  17. Watts RL, Wiegner AW, Young RR. Elastic properties of muscles measured at the elbow in man: II. Patients with parkinsonian rigidity. J Neurol Neurosurg Psychiatry 1986;49:1177-1181
  18. Marusiak J, Kisiel-Sajewicz K, Jaskolska A, Jaskolski A. Higher muscle passive stiffness in Parkinson's disease patients than in controls measured by myotonometry. Arch Phys Med Rehabil 2010;91:800-802
  19. Du LJ, He W, Cheng LG, Li S, Pan YS, Gao J. Ultrasound shear wave elastography in assessment of muscle stiffness in patients with Parkinson's disease: a primary observation. Clin Imaging 2016;40:1075-1080
  20. Le Sant G, Nordez A, Hug F, Andrade R, Lecharte T, McNair PJ, et al. Effects of stroke injury on the shear modulus of the lower leg muscle during passive dorsiflexion. J Appl Physiol (1985) 2019;126:11-22
  21. Miyamoto N, Hirata K, Miyamoto-Mikami E, Yasuda O, Kanehisa H. Associations of passive muscle stiffness, muscle stretch tolerance, and muscle slack angle with range of motion: individual and sex differences. Sci Rep 2018;8:8274
  22. Xu J, Hug F, Fu SN. Stiffness of individual quadriceps muscle assessed using ultrasound shear wave elastography during passive stretching. J Sport Health Sci 2018;7:245-249
  23. Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord 2015;30:1591-1601
  24. Nasirzade A, Ehsanbakhsh A, Ilbeygi S, Sobhkhiz A, Argavani H, Aliakbari M. Relationship between sprint performance of front crawl swimming and muscle fascicle length in young swimmers. J Sports Sci Med 2014;13:550-556
  25. Kruse A, Schranz C, Tilp M, Svehlik M. Muscle and tendon morphology alterations in children and adolescents with mild forms of spastic cerebral palsy. BMC Pediatr 2018;18:156
  26. Gao J, He W, Du LJ, Chen J, Park D, Wells M, et al. Quantitative ultrasound imaging to assess the biceps brachii muscle in chronic post-stroke spasticity: preliminary observation. Ultrasound Med Biol 2018;44:1931-1940
  27. Xiao Y, Wang C, Sun Y, Zhang X, Cui L, Yu J, et al. Quantitative estimation of passive elastic properties of individual skeletal muscle in vivo using normalized elastic modulus-length curve. IEEE Trans Biomed Eng 2020;67:3371-3379
  28. Hug F, Lacourpaille L, Maisetti O, Nordez A. Slack length of gastrocnemius medialis and Achilles tendon occurs at different ankle angles. J Biomech 2013;46:2534-2538
  29. Maisetti 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
  30. Hirata K, Kanehisa H, Miyamoto-Mikami E, Miyamoto N. Evidence for intermuscle difference in slack angle in human triceps surae. J Biomech 2015;48:1210-1213
  31. Powell D, Muthumani A, Xia R. A comparison of the effects of continuous versus discontinuous movement patterns on parkinsonian rigidity and reflex responses to passive stretch and shortening. J Nat Sci 2016;2:e201
  32. Zhou J, Yu J, Liu C, Tang C, Zhang Z. Regional elastic properties of the Achilles tendon is heterogeneously influenced by individual muscle of the gastrocnemius. Appl Bionics Biomech 2019;2019:8452717
  33. Kelly JP, Koppenhaver SL, Michener LA, Proulx L, Bisagni F, Cleland JA. Characterization of tissue stiffness of the infraspinatus, erector spinae, and gastrocnemius muscle using ultrasound shear wave elastography and superficial mechanical deformation. J Electromyogr Kinesiol 2018;38:73-80
  34. S,endur HN, Cindil E, Cerit MN, Kilic P, Gultekin II, Oktar SO. Evaluation of effects of aging on skeletal muscle elasticity using shear wave elastography. Eur J Radiol 2020;128:109038
  35. Akagi R, Yamashita Y, Ueyasu Y. Age-related differences in muscle shear moduli in the lower extremity. Ultrasound Med Biol 2015;41:2906-2912
  36. Alfuraih AM, Tan AL, O'Connor P, Emery P, Wakefield RJ. The effect of ageing on shear wave elastography muscle stiffness in adults. Aging Clin Exp Res 2019;31:1755-1763
  37. Sun Y, Xiao Y, Li F, Wang C, Wu T, Zhou M, et al. Diagnosing muscle atrophy by use of a comprehensive method of assessing the elastic properties of muscle during passive stretching. AJR Am J Roentgenol 2020;214:862-870
  38. Rosskopf AB, Ehrmann C, Buck FM, Gerber C, Fluck M, Pfirrmann CW. Quantitative shear-wave US elastography of the supraspinatus muscle: reliability of the method and relation to tendon integrity and muscle quality. Radiology 2016;278:465-474
  39. Botar-Jid C, Damian L, Dudea SM, Vasilescu D, Rednic S, Badea R. The contribution of ultrasonography and sonoelastography in assessment of myositis. Med Ultrason 2010;12:120-126
  40. Tan AH, Hew YC, Lim SY, Ramli NM, Kamaruzzaman SB, Tan MP, et al. Altered body composition, sarcopenia, frailty, and their clinico-biological correlates, in Parkinson's disease. Parkinsonism Relat Disord 2018;56:58-64
  41. Baumer TG, Davis L, Dischler J, Siegal DS, van Holsbeeck M, Moutzouros V, et al. Shear wave elastography of the supraspinatus muscle and tendon: repeatability and preliminary findings. J Biomech 2017;53:201-204