Ann Rehabil Med.  2023 Dec;47(6):493-501. 10.5535/arm.23091.

Changes in Lower Extremity Muscle Quantity and Quality in Patients with Subacute Stroke

• Kim DH
• Cho ES
• Park YS
• Chang HJ
• Park JG
• Kim JY
• Lee JH

• KMID: 2549730
• DOI: http://doi.org/10.5535/arm.23091

Abstract

Objective
To analyze the changes in muscle mass and quality with time on the paretic and non-paretic sides in subacute stroke patients and identify correlations between the variation of muscle mass and quality and lower limb functions.
Methods
Thirty hemiplegia patients diagnosed with stroke participated in this study. To evaluate poststroke muscle changes, longitudinal measurement of muscle mass and quality was conducted with bilateral lower limbs. The elastic shear modulus was measured using shear wave elastography and muscle thickness (MT) of rectus femoris, vastus intermedius, vastus lateralis (VL), vastus medialis, tibialis anterior, and gastrocnemius (GCM) muscles. Functional evaluation was performed using Berg Balance Scale (BBS), Five Times Sit to Stand Test (FTSST). Follow-up was performed at discharge. The muscle mass and quality were compared according to time. We analyzed whether muscle quantity and quality were related to function.
Results
MT demonstrated no significant change with time. The elastic shear modulus increased significantly in the paretic VL and GCM muscles and did not change significantly in the muscles on the non-paretic side. Correlation analysis detected that elastic shear modulus in the VL has a cross-sectional negative relationship between BBS and positive relationship between FTSST. There were significant correlation between variation of FTSST and the variation of the elastic shear modulus in VL.
Conclusion
Only paretic VL and GCM muscle quality changed in subacute stroke patients and muscle’s property related to lower limb functions. Therefore, the lower extremity requires an approach to muscle quality rather than quantity for subacute stroke patients.

Keyword

Stroke; Skeletal mass; Elasticity imaging techniques; Skeletal muscle; Sarcopenia

Figure

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  Fig. 1. Measurement of thickness or rectus femoris (RF) and vastus intermedius (VI) muscle (A) and elastic shear modulus (B). The circles represent the region of interest (ROI) from which elastic shear modulus (kPa) was measured. The average of eight ROIs was used for analysis.

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  Fig. 2. Cross-sectional correlation between lower limb functions and elastic shear modulus (kPa) of each muscle: rectus femoris (RF) (A), vastus intermedius (VI) (B), vastus medialis (VM) (C), vastus lateralis (VL) (D), tibialis anterior (TA) (E), and gastrocnemius (GCM) (F). BBS, Berg Balance Scale; FTSST, Five Times Sit to Stand Test. *p<0.05.

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  Fig. 3. Relationships between changes in lower limb function and changes in muscle elastic shear modulus. (A, B) vastus lateralis (VL). (C, D) gastrocnemius (GCM). BBS, Berg Balance Scale; FTSST, Five Times Sit to Stand Test. *p<0.05.

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Reference

1. Gittler M, Davis AM. Guidelines for adult stroke rehabilitation and recovery. JAMA. 2018; 319:820–1.

2. Inoue T, Maeda K, Shimizu A, Nagano A, Ueshima J, Sato K, et al. Calf circumference value for sarcopenia screening among older adults with stroke. Arch Gerontol Geriatr. 2021; 93:104290.

3. Shiraishi A, Yoshimura Y, Wakabayashi H, Tsuji Y. Prevalence of stroke-related sarcopenia and its association with poor oral status in post-acute stroke patients: implications for oral sarcopenia. Clin Nutr. 2018; 37:204–7.

4. Scherbakov N, Sandek A, Doehner W. Stroke-related sarcopenia: specific characteristics. J Am Med Dir Assoc. 2015; 16:272–6.

5. Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF. Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002; 83:1703–7.

6. Monjo H, Fukumoto Y, Asai T, Kubo H, Ohshima K, Tajitsu H, et al. Differences in muscle thickness and echo intensity between stroke survivors and age- and sex-matched healthy older adults. Phys Ther Res. 2020; 23:188–94.

7. Berenpas F, Martens AM, Weerdesteyn V, Geurts AC, van Alfen N. Bilateral changes in muscle architecture of physically active people with chronic stroke: a quantitative muscle ultrasound study. Clin Neurophysiol. 2017; 128:115–22.

8. Akazawa N, Harada K, Okawa N, Kishi M, Tamura K, Moriyama H. Changes in quadriceps thickness and echo intensity in chronic stroke survivors: a 3-year longitudinal study. J Stroke Cerebrovasc Dis. 2021; 30:105543.

9. Monjo H, Fukumoto Y, Asai T, Ohshima K, Kubo H, Tajitsu H, et al. Changes in muscle thickness and echo intensity in chronic stroke survivors: a 2-year longitudinal study. J Clin Neurol. 2022; 18:308–14.

10. Matsushita T, Nishioka S, Taguchi S, Yamanouchi A. Sarcopenia as a predictor of activities of daily living capability in stroke patients undergoing rehabilitation. Geriatr Gerontol Int. 2019; 19:1124–8.

11. Yoshimura Y, Wakabayashi H, Bise T, Nagano F, Shimazu S, Shiraishi A, et al. Sarcopenia is associated with worse recovery of physical function and dysphagia and a lower rate of home discharge in Japanese hospitalized adults undergoing convalescent rehabilitation. Nutrition. 2019; 61:111–8.

12. Monjo H, Fukumoto Y, Asai T, Shuntoh H. Muscle thickness and echo intensity of the abdominal and lower extremity muscles in stroke survivors. J Clin Neurol. 2018; 14:549–54.

13. Karabulut M, McCarron J, Abe T, Sato Y, Bemben M. The effects of different initial restrictive pressures used to reduce blood flow and thigh composition on tissue oxygenation of the quadriceps. J Sports Sci. 2011; 29:951–8.

14. Abe T, Yoshimura Y, Sato Y, Nagano F, Matsumoto A. Validity of sarcopenia diagnosis defined by calf circumference for muscle mass to predict functional outcome in patients with acute stroke. Arch Gerontol Geriatr. 2023; 105:104854.

15. Jakubowski KL, Terman A, Santana RVC, Lee SSM. Passive material properties of stroke-impaired plantarflexor and dorsiflexor muscles. Clin Biomech (Bristol, Avon). 2017; 49:48–55.

16. Brandenburg JE, Eby SF, Song P, Zhao H, Brault JS, Chen S, et al. Ultrasound elastography: the new frontier in direct measurement of muscle stiffness. Arch Phys Med Rehabil. 2014; 95:2207–19.

17. Lee SS, Spear S, Rymer WZ. Quantifying changes in material properties of stroke-impaired muscle. Clin Biomech (Bristol, Avon). 2015; 30:269–75.

18. Cortez CD, Hermitte L, Ramain A, Mesmann C, Lefort T, Pialat JB. Ultrasound shear wave velocity in skeletal muscle: a reproducibility study. Diagn Interv Imaging. 2016; 97:71–9.

19. 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; 44:1931–40.

20. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: validation of an instrument. Can J Public Health. 1992; 83 Suppl 2:S7–11.

21. Lee SSM, Jakubowski KL, Spear SC, Rymer WZ. Muscle material properties in passive and active stroke-impaired muscle. J Biomech. 2019; 83:197–204.

22. Rasool G, Wang AB, Rymer WZ, Lee SSM. Shear waves reveal viscoelastic changes in skeletal muscles after hemispheric stroke. IEEE Trans Neural Syst Rehabil Eng. 2018; 26:2006–14.

23. Mathevon L, Michel F, Aubry S, Testa R, Lapole T, Arnaudeau LF, et al. Two-dimensional and shear wave elastography ultrasound: a reliable method to analyse spastic muscles? Muscle Nerve. 2018; 57:222–8.

24. Wu CH, Ho YC, Hsiao MY, Chen WS, Wang TG. Evaluation of post-stroke spastic muscle stiffness using shear wave ultrasound elastography. Ultrasound Med Biol. 2017; 43:1105–11.

25. Burke D, Wissel J, Donnan GA. Pathophysiology of spasticity in stroke. Neurology. 2013; 80(3 Suppl 2):S20–6.

26. Lieber RL, Ward SR. Cellular mechanisms of tissue fibrosis. 4. Structural and functional consequences of skeletal muscle fibrosis. Am J Physiol Cell Physiol. 2013; 305:C241–52.

27. 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.

28. Carin-Levy G, Greig C, Young A, Lewis S, Hannan J, Mead G. Longitudinal changes in muscle strength and mass after acute stroke. Cerebrovasc Dis. 2006; 21:201–7.

29. Ramnemark A, Nyberg L, Lorentzon R, Englund U, Gustafson Y. Progressive hemiosteoporosis on the paretic side and increased bone mineral density in the nonparetic arm the first year after severe stroke. Osteoporos Int. 1999; 9:269–75.

30. Celik B, Ones K, Ince N. Body composition after stroke. Int J Rehabil Res. 2008; 31:93–6.