Spasticity is a frequent and disabling post-stroke sequela, with an estimated prevalence of 25% 1. Despite being a well-known disorder, there is little consensus on how to measure spasticity 2. Subjective scales are common in the clinical setting, with limited evidence to support their use, as they lack proper validity 3, reliability and reproducibility 4. Clinical measures cannot discriminate either between the neural and non-neural (peripheral) components of spasticity 4, except the Modified Tardieu Scale (MTS). The peripheral contribution to post-stroke spasticity (PSS) can be quantified for clinical and research purposes, using objective, non-invasive methods, e.g., shear-wave elastography and myotonometry 4,5. Myotonometry represents a valid, reliable, and convenient tool 4,6 that has proven to be useful to monitor PSS following conservative or invasive treatments 7. However, current evidence on the ability of myotonometry to discriminate between spastic and non-spastic muscles after stroke is scarce and conflicting 6. It has been recommended to conduct myotonometry measurement of PSS at several muscle sites of testing and in different muscle positions, i.e., relaxed or stretched 6, to get a clear picture of how muscle mechanical properties may change after stroke 8 and in response to rehabilitation programs.
This study aimed to investigate the differences in myotonometry scores for muscle tone and stiffness in stroke patients, comparing sides (affected vs. non-affected), sites (muscle belly vs. musculotendinous), and groups (subacute stroke, chronic stroke, and control), during two evaluation protocols (relaxed or stretched muscle). As a secondary goal, we analyzed the possible associations between myotonometry and the MTS. We hypothesized differences between protocols in myotonometry scores and that measuring tone and stiffness in stretched position would help to better distinguish between the affected and non-affected sides in stroke patients, and between individuals with or without stroke.
1. Zeng H, Chen J, Guo Y, Tan S. Prevalence and Risk Factors for Spasticity After Stroke: A Systematic Review and Meta-Analysis. Front. Neurol. 2021;11. DOI: 10.3389/fneur.2020.616097.
2. Lehoux MC, Sobczak S, Cloutier F, Charest S, Bertrand-Grenier A. Shear wave elastography potential to characterize spastic muscles in stroke survivors: Literature review. Clin Biomech. 2020;72:84–93. DOI: 10.1016/j.clinbiomech.2019.11.025.
3. Aloraini SM, Gäverth J, Yeung E, MacKay-Lyons M. Assessment of spasticity after stroke using clinical measures: A systematic review. Disabil Rehabil. 2015;37:2313–23. DOI: 10.3109/09638288.2015.1014933.
4. Luo Z, Lo WLA, Bian R, Wong S, Li L. Advanced quantitative estimation methods for spasticity: a literature review. J Int Med Res. 2019;48. DOI: 10.1177/0300060519888425
5. Tran A, Gao J. Quantitative Ultrasound to Assess Skeletal Muscles in Post Stroke Spasticity. J Cent Nerv Syst Dis. 2021;13. DOI: 10.1177/1179573521996141
6. García-Bernal MI, Heredia-Rizo AM, González-García P, Cortés-Vega MD, Casuso-Holgado MJ. Validity and reliability of myotonometry for assessing muscle viscoelastic properties in patients with stroke: A systematic review and meta-analysis. Sci Rep. 2021;11 (1):5062. DOI: 10.1038/s41598-021-84656-1
7. Megna M, Marvulli R, Farì G, Gallo G, Dicuonzo F, Fiore P, et al. Pain and Muscles Properties Modifications After Botulinum Toxin Type A (BTX-A) and Radial Extracorporeal Shock Wave (rESWT) Combined Treatment. Endocr Metab Immune Disord Drug Targets. 2019;19(8):1127-1133. DOI: 10.2174/1871530319666190306101322.
8. Burridge JH, Wood DE, Hermens HJ, Voerman GE, Johnson GR, van Wijck F, et al. Theoretical and methodological considerations in the measurement of spasticity. Disabil Rehabil. 2005;27:69–80. DOI: 10.1080/09638280400014592.
9. Chuang LL, Wu CY, Lin KC, Lur SY. Quantitative mechanical properties of the relaxed biceps and triceps brachii muscles in patients with subacute stroke: A reliability study of the Myoton-3 myometer. Stroke Res Treat. 2012;2012. DOI: 10.1155/2012/617694.
10. Sarasso S, Määttä S, Ferrarelli F, Poryazova R, Tononi G, Small SL. Plastic changes following imitation-based speech and language therapy for aphasia: A high-density sleep EEG study. Neurorehabil Neural Repair. 2014;28:129–38. DOI: 10.1177/1545968313498651.
11. Ansari N, Naghdi S, Arab T, Jalair S. The interrater and intrarater reliability of the Modified Ashworth Scale in the assessment of muscle spasticity: limb and muscle group effect. NeuroRehabilitation. 2008;23:231–7. DOI: 10.1177/1545968313498651.
12. Shu X, McConaghy C, Knight A. Validity and reliability of the Modified Tardieu Scale as a spasticity outcome measure of the upper limbs in adults with neurological conditions: A systematic review and narrative analysis. BMJ Open. 2021;11:1–10. DOI: 10.1136/bmjopen-2021-050711
13. Bohannon R, Smith M. Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys. Ther. 1987;67:206–7. DOI: 10.1093/ptj/67.2.206
14. Quinn TJ, Elliott E, Langhorne P. Cognitive and mood assessment tools for use in stroke. Stroke. 2018;49 (2):483–90. DOI: 10.1161/STROKEAHA.117.016994.
15. Ilahi S, T. Masi A, White A, Devos A, Henderson J, Nair K. Quantified biomechanical properties of lower lumbar myofascia in younger adults with chronic idiopathic low back pain and matched healthy controls. Clin. Biomech. 2020;73:78–85. DOI: 10.1016/j.clinbiomech.2019.12.026
16. Paulis WD, Horemans HLD, Brouwer BS, Stam HJ. Excellent test-retest and inter-rater reliability for Tardieu Scale measurements with inertial sensors in elbow flexors of stroke patients. Gait Posture. 2011;33 (2):185–9. DOI: 10.1016/j.gaitpost.2010.10.094.
17. Petek Balci B. Spasticity Measurement. Arch Meuropychiatry. 2018; 55: S49–53. DOI: 10.29399/npa.23339.
18. Puce L, Currà A, Marinelli L, Mori L, Capello E, Di Giovanni R, et al. Clinical Neurophysiology Practice Spasticity, spastic dystonia, and static stretch reflex in hypertonic muscles of patients with multiple sclerosis. Clin Neurophysiol Pract. 2021;6:194–202. DOI: 10.1016/j.cnp.2021.05.002.
19. Eby SF, Zhao H, Song P, Vareberg BJ, Kinnick RR, Greenleaf JF, et al. Quantifying spasticity in individual muscles using shear wave elastography. Radiol Case Reports. 2017;12 (2):348–52. DOI: 10.1016/j.radcr.2017.01.004.
20. Amirova LE, Plehuna A, Rukavishnikov I V., Saveko AA, Peipsi A, Tomilovskaya ES. Sharp Changes in Muscle Tone in Humans Under Simulated Microgravity. Front Physiol. 2021;12:1–12. DOI: 10.3389/fphys.2021.661922.
21. Xiaoyan L, Shin H, Zong Y, Li S, Zhou P. Assessing muscle compliance in stroke with the Myotonometer. Clin Biomech. 2017;50:110–3. DOI: 10.1016/j.clinbiomech.2017.10.013.
22. Condliffe EG, Clark DJ, Patten C. Reliability of elbow stretch reflex assessment in chronic post-stroke hemiparesis. Clin Neurophysiol. 2005;116 (8):1870–8. DOI: 10.1016/j.clinph.2005.02.030.
23. 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 (9):1931–40. DOI: 10.1016/j.ultrasmedbio.2017.12.012.
24. Davis JF, Khir AW, Barber L, Reeves ND, Khan T, DeLuca M, et al. The mechanisms of adaptation for muscle fascicle length changes with exercise: Implications for spastic muscle. Med Hypotheses. 2020;144:110199. DOI: 10.1016/j.mehy.2020.110199.
25. Lakie M, Campbell KS. Muscle thixotropy—where are we now? J Appl Physiol. 2019;126 (6):1790–9. DOI: 10.1152/japplphysiol.00788.2018.
26. Vattanasilp W, Ada L, Crosbie J. Contribution of thixotropy, spasticity, and contracture to ankle stiffness after stroke. J Neurol Neurosurg Psychiatry. 2000;69 (1):34–9. DOI: 10.1136/jnnp.69.1.34.
27. Bakheit AMO. The pharmacological management of post-stroke muscle spasticity. Drugs and Aging. 2012;29 (12):941–7. DOI: 10.1007/s40266-012-0034-z.
28. 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 (3):C241-52. DOI: 10.1152/ajpcell.00173.2013.
29. Leonard CT, Stephens JU, Stroppel SL. Assessing the spastic condition of individuals with upper motoneuron involvement: Validity of the Myotonometer. Arch Phys Med Rehabil. 2001;82 (10):1416–20. DOI: 10.1053/apmr.2001.26070.
30. Rydahl SJ, Brouwer BJ. Ankle stiffness and tissue compliance in stroke survivors: A validation of Myotonometer measurements. Arch Phys Med Rehabil. 2004;85:1631–7. DOI: 10.1016/j.apmr.2004.01.026.
31. Li X, Shin H, Li S, Zhou P. Assessing muscle spasticity with Myotonometric and passive stretch measurements: Validity of the Myotonometer. Sci Rep. 2017;7:1–7. DOI: 10.1038/srep44022.
32. Leng Y, Lo WLA, Hu C, Bian R, Xu Z, Shan X, et al. The Effects of Extracorporeal Shock Wave Therapy on Spastic Muscle of the Wrist Joint in Stroke Survivors: Evidence From Neuromechanical Analysis. Front Neurosci. 2021;14:1–16. DOI: 10.3389/fnins.2020.580762.
33. Miller T, Ying MTC, Chung RCK, Pang MYC. Convergent Validity and Test-Retest Reliability of Multimodal Ultrasonography and Related Clinical Measures in People With Chronic Stroke. Arch Phys Med Rehabil. 2021; 23;S0003-9993 (21)01496-9. DOI: 10.1016/j.apmr.2021.09.015.
34. Wu C-H, Ho Y-C, Hsiao M-Y. Evaluation of Post-Stroke Spastic Muscle Stiffness Using Shear Wave Ultrasound Elastography. Ultrasound Med Biol. 2017;43 (6):1105–11. DOI: 10.1016/j.ultrasmedbio.2016.12.008.
35. Haugh A, Pandyan A, Johnson G. A systematic review of the Tardieu Scale for the measurement of spasticity. Disabil Rehabil. 2006;28 (15):899–907. DOI: 10.1080/09638280500404305.
36. Chuang LL, Wu CY, Lin KC. Reliability, validity, and responsiveness of myotonometric measurement of muscle tone, elasticity, and stiffness in patients with stroke. Arch Phys Med Rehabil. 2012;93 (3):532–40. DOI: 10.1016/j.apmr.2011.09.014.
37. Fröhlich-Zwahlen AK, Casartelli NC, Item-Glatthorn JF, Maffiuletti NA. Validity of resting myotonometric assessment of lower extremity muscles in chronic stroke patients with limited hypertonia: A preliminary study. J Electromyogr Kinesiol. 2014;24:762–9. DOI: 10.1016/j.jelekin.2014.06.007.
38. Wang J-SS, Lee S-B Bin, Moon S-HH. The immediate effect of PNF pattern on muscle tone and muscle stiffness in chronic stroke patient. J Phys Ther Sci. 2016;28:967–70. DOI: 10.1589/jpts.28.967.
39. Lo WLA, Zhao JL, Li L, Mao YR, Huang DF. Relative and Absolute Interrater Reliabilities of a Hand-Held Myotonometer to Quantify Mechanical Muscle Properties in Patients with Acute Stroke in an Inpatient Ward. Biomed Res Int. 2017;2017. DOI: 10.1155/2017/4294028.
40. 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. DOI: 10.1016/j.clinph.2016.10.096.
41. Lee S, Spear S, Rymer W. Quantifying changes in material properties of stroke-impaired muscle. Clin Biomech. 2015;30 (3):269–275. DOI: 10.1016/j.clinbiomech.2015.01.004.
42. Mirbagheri MM, Tsao C, Rymer WZ. Natural history of neuromuscular properties after stroke: A longitudinal study. J Neurol Neurosurg Psychiatry. 2009 (11);80:1212–7. DOI: 10.1136/jnnp.2008.155739.
43. Marusiak J, Jaskólska A, Budrewicz S, Koszewicz M, Jaskólski A. Increased muscle belly and tendon stiffness in patients with Parkinson's disease, as measured by myotonometry. Mov Disord. 2011;26 (11):2119–22. DOI: 10.1002/mds.23841.
44. Ge JS, Chang TT, Zhang ZJ. Reliability of myotonometric measurement of stiffness in patients with spinal cord injury. Med Sci Monit. 2020;26:1–7. DOI: 10.12659/MSM.924811.
45. Ko C-YY, Choi H-JJ, Ryu J, Kim G. Between-day reliability of MyotonPRO for the non-invasive measurement of muscle material properties in the lower extremities of patients with a chronic spinal cord injury. J Biomech. 2018;73:60–5. DOI: 10.1016/j.jbiomech.2018.03.026.
46. Feng YN, Li YP, Liu CL, Zhang ZJ. Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO. Sci Rep. 2018;8:1–9. DOI: 10.1038/s41598-018-34719-7.
47. Huang J, Qin K, Tang C, Zhu Y, Klein CS, Zhang Z, et al. Assessment of passive stiffness of medial and lateral heads of gastrocnemius muscle, achilles tendon, and plantar fascia at different ankle and knee positions using the myotonPRO. Med Sci Monit. 2018;24:7570–6. DOI: 10.12659/MSM.909550.
48. Theis N, Mohagheghi AA, Korff T. Mechanical and material properties of the plantarflexor muscles and Achilles tendon in children with spastic cerebral palsy and typically developing children. J Biomech. 2016;49:3004–8. DOI: 10.1016/j.jbiomech.2016.07.020.
49. Faturi FM, Lopes Santos G, Ocamoto GN, Russo TL. Structural muscular adaptations in upper limb after stroke: a systematic review. Top Stroke Rehabil. 2019;26 (1):73–9. DOI: 10.1080/10749357.2018.1517511.
50. Chardon MK, Suresh NL, Dhaher YY, Rymer WZ. In-Vivo Study of Passive Musculotendon Mechanics in Chronic Hemispheric Stroke Survivors. IEEE Trans Neural Syst Rehabil Eng. 2020;28 (4):1022–31. DOI: 10.1109/TNSRE.2020.2972206.
51. Narici M V., Maganaris CN. Plasticity of the muscle-tendon complex with disuse and aging. Exerc Sport Sci Rev. 2007;35 (3):126–34. DOI: 10.1097/jes.0b013e3180a030ec.
52. Chang TT, Feng YN, Zhu Y, Liu CL, Wang XQ, Zhang ZJ. Objective assessment of regional stiffness in achilles tendon in different ankle joint positions using the MyotonPRO. Med Sci Monit. 2020;26:1–8. DOI: 10.12659/MSM.926407.
53. Bernhardt J, Hayward KS, Kwakkel G, Ward NS, Wolf SL, Borschmann K, et al. Agreed definitions and a shared vision for new standards in stroke recovery research: The Stroke Recovery and Rehabilitation Roundtable taskforce. Int. J. Stroke. 2017;12:444–50. DOI: 10.1177/1747493017711816.
54. Nichols-Larsen DS, Clark PC, Zeringue A, Greenspan A, Blanton S. Factors influencing stroke survivors’ quality of life during subacute recovery. Stroke. 2005;36:1480–4. DOI: 10.1161/01.STR.0000170706.13595.4f.
55. Patrick E, Ada L. The Tardieu Scale differentiates contracture from spasticity whereas the Ashworts Scale is confounded by it. Clin. Rehabil. 2006;20:173–81. DOI: 10.1191/0269215506cr922oa.
56. Chen CL, Chen CY, Chen HC, Wu CY, Lin KC, Hsieh YW, et al. Responsiveness and minimal clinically important difference of modified ashworth scale in patients with stroke. Eur. J. Phys. Rehabil. Med. 2019;55:754–60. DOI: 10.23736/S1973-9087.19.05545-X.