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Measuring mechanical properties of spastic muscles after stroke. Does muscle position during assessment really matter?

Open AccessPublished:June 17, 2022DOI:https://doi.org/10.1016/j.apmr.2022.05.012

      HIGHLIGHTS

      • Measuring in stretched position with Myoton helps to discriminate spastic muscle.
      • Clinical measure of spasticity with the MTS was not correlated with myotonometry.
      • Muscles properties change in stroke survivors at different stages.

      Abstract

      Objective

      To investigate the influence of muscle position (relaxed vs. stretched) on muscle mechanical properties and the ability of myotonometry to detect differences between sides, groups, and sites of testing in stroke patients. We also analyzed the association between myotonometry and clinical measures of spasticity.

      Design

      Cross-sectional study.

      Setting

      Outpatient rehabilitation units including private and public centers.

      Participants

      Seventy-one participants (20 subacute stroke, 20 chronic stroke, and 31 controls) were recruited.

      Intervention

      Muscle mechanical properties were measured bilaterally with a MyotonPRO at muscle belly and musculotendinous sites during two protocols (muscle relaxed or in maximal bearable stretched position).

      Main outcome measure

      Muscle tone and stiffness of the biceps brachii and gastrocnemius. Post-stroke spasticity was evaluated with the Modified Tardieu Scale (MTS). A mixed-model analysis of variance (ANOVA) was used to detect differences in the outcome measures.

      Results

      The ANOVA showed a significant effect of muscle position on muscle mechanical properties (higher tone and stiffness with the muscle assessed in stretched position). Measurements with the stretched muscle could help discriminate between spastic and non-spastic sides, but only at the biceps brachii. Overall, there was significant increase in tone and stiffness, in the chronic stroke group, and in myotendinous sites, compared to muscle belly sites (all, P < .05). No correlations were found between myotonometry and the MTS.

      Conclusion

      Myotonometry assessment of mechanical properties with the muscle stretched, improves the ability of myotonometry to discriminate between sides in patients after stroke, and between people with and without stroke.

      Keywords

      List of abbreviations

      MB
      Muscle belly
      MT
      Musculotendinous
      MTS
      Modified Tardieu Scale
      PSS
      Post stroke spasticity
      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.

      Methods

       Design

      We conducted a multicenter, cross-sectional study, including adults with subacute (between 6 - 36 weeks after the event) 9, or chronic (more than 36 weeks) stroke 10, and healthy participants. The protocol of the study respected the ethical guidelines set in the Helsinki Declaration, and was approved by the Junta de Andalucía Ethical Committee for Biomedical Research (CI 1222-N-16). It followed the STROBE framework for observational studies. All participants provided verbal and written informed consent.

       Participants

      Individuals with a first-ever stroke were selected from public and private centers. Participants should have, at least, a slight increase of biceps brachii and gastrocnemius muscle tone. This was identified with a score ≥ 1 in the Modified Ashworth Scale 11, which addresses the involuntary muscle activation feature of spasticity 12, as the resistance to a passive movement 13. The exclusion criteria were as follows: cognitive impairtment (score > 24 in the Mini-Mental State Examination) 14; a diagnosed mood disorder or other neurological condition; prior severe upper or lower limb trauma; changes in medication for PSS in the previous 48h; treatment with botulinum toxin injections within twelve weeks or during the study period; and an epileptic crisis during the previous week. Those in the healthy control group were recruited from the same population-based cohort.

       Outcome measures

      Muscle tone and dynamic stiffness of the biceps brachii and gastrocnemius were assessed with a MyotonPRO (Myoton AS, Tallinn, Estonia) 6. The device contains a probe that applies an initial load of 0.18 N to the skin, and then adds up consecutive short impulses (0.40 N) to the subcutaneous tissue to characterize mechanical properties. The MyotonPRO calculates muscle tone (tension) measuring the natural frequency of the acceleration signal, and muscle stiffness measuring the damped natural oscillation response, using an accelerometer 15. Measurements were taken bilaterally at muscle belly (MB) and musculotendinous (MT) sites, with the muscle relaxed or in the maximum bearable stretched position. The mean score of the two measures was used for the analysis. Regarding the biceps brachii analysis, participants started in relaxed supine position, with the elbow flexed at 45° and forearm in neutral position. For analysing the gastrocnemius, participants lied in prone with approximately 45° of knee flexion. Three sites of muscle testing were included, namely one MT location and two MB sites. For MB, the mean value at the two sites was employed in the analysis.
      The level of PSS was measured with the MTS 16, which adressess the muscle response to a manual stretch elicited as slow as possible (V1), and as fast as possible (V3). At fast stretch, muscle tone reflex increases and it is felt at a so-called ‘catch angle’. V1 denotes the passive joint range of movement, whereas V3 denotes the catch angle used to assess spasticity. V1 and V3 were quantified with an electrogoniometer (Biometrics Ltd, Gwent, UK). At V3, the quality of muscle reaction was scored from 0 to 5, where 0 represents no resistance during passive motion, and 5 represents that the joint cannot be moved 17. To conduct the MTS at the biceps brachii, participants were in supine and the elbow was initially positioned in maximal flexion and supination. For the lower limb, participants remained in prone with knees fully extended and feet outside the table.
      All outcomes were collected by the same examiner, who had over 10 years of experience in neurorehabilitation using clinical measures, and was previously trained with the MyotonPRO. The examiner remained unaware of the study aims and the participants’ allocation group.

       Statistical Analysis

      Sample size was calculated with the G*Power software (v. 3.1.9.2, Heinrich-Heine University, Düsseldorf, Germany). We assumed an alpha level of .05, an 80% statistical power, and a high effect size (η2 = 0.15) for differences between groups on muscle tone and stiffness. This generated a sample of 19 participants per group.
      Statistical processing was conducted with the PASW Advanced Statistics (SPSS Inc, Chicago, IL), version 26.0. Normal distribution of the data was evaluated with the Shapiro-Wilk test. We used a mixed-model analysis of variance ANOVA to compare differences in tone and stiffness of the biceps brachii and gastrocnemius, using muscle position (relaxed vs. stretched), side (affected vs. non-affected) and site (MB vs. MT) as the within-subject factors, and group (subacute stroke, chronic stroke, and controls) as the between-subject factor. The Spearman's rank test or the Pearson product-moment correlation coefficient analysis were used to test for associations between myotonometry measurement and the MTS. The level of significance was set to P < 0.05.

       Data availability

      The data that support the study findings are available from the corresponding author upon request.

      Results

      Seventy-one participants (20 subacute stroke, 20 chronic stroke, and 31 controls) were recruited (figure 1). The clinical and demographic characteristics of the sample are listed in table 1.
      Figure 1
      Figure 1Flowchart diagram of the study participants.
      Table 1Baseline clinical and demographic features of participants
      Subacutestroke (n=20)Chronicstroke (n=20)Control group (n=31)Pvalue
      Age (yrs)60.2 ± 9.761.45 ± 9.760.8 ± 10.60.926
      Sex, female, % (n)35% (7)35% (7)45.2% (14)0.689
      Time after stroke (weeks)17 (6 - 34)242.5 (58 - 1108)N/A< 0.001
      Affected side, left, % (n)55% (11)75% (15)N/A0.289
      Hand dominance, right,

      left, ambidextrous, % (n)
      100% (20)

      85% (17);

      5% (1); 10% (2)
      80.6% (25);

      19.4% (6)
      0.131

      Leg dominance, right,

      left, ambidextrous, % (n)
      95% (19);

      5% (1);
      80% (16);

      5% (1); 15% (3)
      83.9% (26);

      16.1% (5)
      0.319

      Data are expressed as mean ± standard deviation, in percentage (%), or as median and (interquartile range).

       Comparison between measurement protocols

      Tables 2 and 3 include the tone and stiffness values at the different sites, sides, and groups during the evaluation protocols. The ANOVA revealed a significant effect of muscle position during myotonometry assessment (relaxed vs. stretched) on muscle mechanical properties for: (a) the biceps brachii: tone, F = 59.567, P < .001, η2 = .095; stiffness, F = 22.808, P < .001, η2 = .039; and (b) the gastrocnemius: tone, F = 313.2, P < .001; η2 = .365; stiffness: F = 341.57; P < .001; η2 = .386. Overall, scores were significantly higher bilaterally and in most testing sites with the muscle stretched than with the muscle relaxed (with a large effect size).
      Table 2Muscle tone (Hz) and stiffness (N/m) for the biceps brachii at the different sites, sides, and groups during the two measurement protocols
      Subacute stroke groupChronic stroke groupControl Group
      SideMuscle positionToneStiffnessToneStiffnessToneStiffness
      MB sitesDominant / Non-affectedRelaxed

      Stretched
      14.2 ± 1.8

      15.0 ± 1.9 *
      259.1 ± 53.3

      267.6 ± 50.7
      14.8 ± 1.5

      15.3 ± 1.9 *
      271.6 ± 40.7

      276.4 ± 44.8 *
      14.7± 2.1

      15.7± 2.4 *
      271.2 ± 48.7

      289.3 ± 53.4 *
      Non-dominant / AffectedRelaxed

      Stretched
      15.8 ± 2.5

      16.2 ± 2.3
      312.3 ± 74.2

      309.2 ± 64.3
      15.6 ± 2.1

      16.7 ± 2.7 *
      301.5 ± 60.2

      315.9 ± 68.3
      14.6 ±1.8

      15.6 ± 2.0 *
      276.3 ± 44.6

      291.9 ± 43.4 *
      MT sitesDominant / Non-affectedRelaxed

      Stretched
      14.3 ±1 .3

      16.4 ± 1.8 *
      245.6 ± 33.2

      285.3 ± 48.7 *
      15.1 ± 2.9

      16.4 ± 2.3 *
      275.7 ± 75.2

      290.7 ± 51.8
      14.3 ± 1.5

      16.2 ± 1.7 *
      253.4 ± 39.7

      282.41 ± 36.0 *
      Non-dominant / AffectedRelaxed

      Stretched
      14.4 ± 2.5

      16.2 ± 2.3 *
      251.9 ± 54.2

      285.3 ± 62.7 *
      14.2 ± 1.7

      16.3 ± 2.5 *
      259.9 ± 39.1

      307.9 ± 58.7 *
      14.5 ± 1.9

      16.3 ± 2.1 *
      258.4 ± 48.4

      288.4 ± 50.1 *
      * Indicates significant differences in the within-groups analysis when comparing scores at the same site and side between the two different protocols (muscle relaxed vs. stretched). Abbreviations: MB, muscle belly; MT, myotendinous.
      Table 3Muscle tone (Hz) and stiffness (N/m) for the gastrocnemius at the different sites, sides, and groups during the two measurement protocols
      Subacute stroke groupChronic stroke groupControl Group
      SideMuscle positionToneStiffnessToneStiffnessToneStiffness
      MB sitesDominant / Non-affectedRelaxed

      Stretched
      14.8 ± 1.3

      18.8 ± 2.6 *
      281.8 ± 28.7

      348.4 ± 50.8 *
      16.4 ± 1.9

      20.1 ± 3.4 *
      291.8 ± 35.8

      387.9 ± 93.7 *
      15.3 ± 1.1

      19.8 ± 2.2 *
      285.6 ± 18.1

      383.3 ± 65.2 *
      Non-dominant / AffectedRelaxed

      Stretched
      15.1 ± 1.9

      19.0 ± 3.1 *
      283.3 ± 24.7

      350.2 ± 56.4 *
      16.7 ± 2.9

      19.7 ± 3.3 *
      321.0 ± 58.2

      386.6 ± 106.2 *
      15.6 ± 1.4

      19.8 ± 2.5 *
      286.2 ± 21.4

      375.4 ± 64.4 *
      MT sitesDominant / Non-affectedRelaxed

      Stretched
      21.9 ± 2.4

      26.8 ± 4.4 *
      442.2 ± 56.3

      594.6 ± 123.7 *
      22.8 ± 4.0

      27.6 ± 3.1 *
      468.5 ± 94.5

      620.1 ± 103.4 *
      23.9 ± 3.3

      30.3 ± 4.6 *
      483.2 ± 58.6

      697.6 ± 128.5 *
      Non-dominant / AffectedRelaxed

      Stretched
      21.8 ± 2.9

      27.0 ± 4.7 *
      433.3 ± 63.9

      577.6 ± 132.8 *
      23.0 ± 3.1

      27.1 ± 3.3 *
      459.4 ± 75.9

      599.2 ± 104.2 *
      23.5 ± 2.6

      28.9 ± 3.7 *
      482.5 ± 56.5

      659.8 ± 113.5 *
      * Indicates significant differences in the within-groups analysis when comparing scores at the same site and side between the two different protocols (muscle relaxed vs. stretched). Abbreviations: MB, muscle belly; MT, myotendinous

       Discriminative ability between spastic and non-spastic muscles

      Myotonometry measurements in relaxed position could not discriminate between the affected and non-affected sides or between stroke patients and controls (all, P > .05), except for the lower limb, where higher values were found in the chronic stroke and control groups compared to those with subacute stroke (all, P < .05). For assessments in stretched position, differences between sides were only reported at the biceps brachii (increased stiffness in the spastic side, P = .020). Furthermore, the comparison between groups demonstrated: (a) higher biceps brachii stiffness in the chronic stroke than in the control group (P = .045); and (b) lower gastrocnemius tone and stiffness in participants with subacute stroke compared with healthy controls (all, P < .05).

       Discriminative ability between sites of testing

      There was a significant muscle position*sites interaction, with a moderate to large effect size, for: (a) the biceps brachii: tone, F = 8.158, P < .004, η2 = .015; stiffness, F = 6.330, P < .012, η2 = .012; and (b) the gastrocnemius: tone, F = 6.089, P < .014, η2 = .011; stiffness: F = 39.847, P < .001, η2 = .068. Differences between sites of testing were found in the two protocols, with higher tone and stiffness at MT sites, compared to MB sites (all, P < .05), except for the biceps brachii when measured in relaxed position that showed the opposite trend.

       Correlations

      Table 4 lists the clinical data for the measure of spasticity with the MTS in the stroke groups. No significant correlations were observed between myotonometry and the level of PSS, as assessed with the MTS (all, P > .05).
      Table 4Descriptive data for the clinical measure of spasticity with the Modified Tardieu Scale in the subacute and chronic stroke groups
      Subacute stroke groupChronic stroke group
      V1V3V1 - V3XV1V3V1 – V3X
      Biceps Brachii172.7 ± 3.6118.1 ± 6.254.5 ± 5.92.1 ± 0.1172.1 ± 3.4120.0 ± 5.852.1 ± 5.31.9 ± 0.1
      Gastrocnemius83.1 ± 2.765.5 ± 2.417.6 ± 2.62.3 ± 0.178.5 ± 3.560.1 ± 4.118.4 ± 2.32.4 ± 0.1
      V1: joint angle at slow passive stretch (degrees); V3: ‘catch angle’ at fast passive stretch (degrees); X, quality of muscle reaction at V3, from 0 to 5

      Discussion

      The present findings partly agree with our hypotheses. Tone and stiffness values changed among the two protocols, and myotonometry measurement with the muscle stretched could discriminate between the spastic and non-spastic sides, although only for the biceps brachii. When comparing groups, our results differed depending on the protocol and the assessed muscle. This distinct behavior has been explained on the basis of the different activation patterns of flexor and extensor muscles 18.

       Comparison between measurement protocols

      Myotonometry is a valid and easy-to-use approach to objectively quantify muscle mechanical properties in people after stroke 4,6. However, its high environmental sensitivity 4, the large within- and between-subjects variability 19, together with assessment-related aspects, such as muscle position and operator's experience 4,20, stress the importance of agreeing on a standardized evaluation protocol.
      Most previous research in stroke patients has been conducted carrying out myotonometry measurements with the muscle relaxed. Our findings support the notion that muscle position, relaxed or not, can affect myotonometry scores, which depend on the tissue displacement-force relation 21. In our study, we mostly observed higher tone and stiffness during evaluation with the muscle stretched. There are plausible reasons to understand this observation. Motor neuron responsiveness to passive stretch is increased after stroke 22, which may become more evident with the muscle stretched than relaxed 23. PSS is also related with shorter muscle fascicles and more compliant tendons that do not respond properly to stretch, increasing tone and stiffness 24. Additionally, thixotropy, as the influence of movement and time of recovery after movement on mechanical properties 25, is altered after stroke 26 and can modify stiffness 25 and contribute to intrinsic hypertonia 27. All in all, changes in mechanical properties after stroke are linked to changes in muscle morphology and composition 28. This needs to be considered when assessing PSS with myotonometry. It could also explain the lack of association between myotonometry and clinical measures of spasticity, in line with former research 21, but in contradiction with studies that used myotonometry with the muscle contracted 29,30. The scarce and contradictory literature on this issue, and the differences among studies in myotonometry devices and muscle position, can account for the lack of agreement.

       Discriminative ability between spastic and non-spastic muscles

      In stroke patients, myotonometry could only discriminate between sides with the muscle stretched and at the upper limb. In agreement with most literature on the topic 21,31–33, we observed higher stiffness at the spastic biceps brachii, compared with the non-spastic side. It has been argued that stretching of the biceps brachii evokes higher resistance to elbow extension 23, and this can make the muscle stiffer and increase tone 34,35. Nonetheless, evidence on this issue is still preliminary and inconsistent 36. For the gastrocnemius, myotonometry revealed no differences between sides in any of the protocols. These results agree with previous research using myotonometry to analyze the mechanical properties of different lower limb muscles 33,37–39 in individuals with acute 39 or chronic stroke 33,37,38. Bilateral adaptations of the lower limbs, especially in those who remain non physically active after stroke 40, could explain the lack of discriminative ability at the gastrocnemius.
      As regards the comparison between spastic and healthy control muscles, higher tone and stiffness are often expected in chronic post-stroke stages 37,38, although the changes in mechanical properties seem to depend on the assessed muscles 37,38. As in the present study, biceps brachii tone and stiffness have shown to be increased in patients with chronic stroke 23,41. Our findings, however, differed for the lower limb, with no differences between the control and chronic stroke groups, and with lower tone and stiffness in those with subacute stroke. The reduced stiffness at early stages after stroke has been attributed to a low level of functional recovery 42. Therefore, the clinical implications may be different for the upper and lower limbs and in patients with different levels of functionality. Future research should include subgroups of participants with different PSS severity and presentation to answer this question 33.

       Discriminative ability between sites of testing

      Current literature suggests that spatial distribution of mechanical properties may not be homogeneous in spastic muscles. Consistent with this, tone and stiffness were significantly different at MT than at MB sites, for both muscles and assessment protocols. The general trend was towards higher tone and stiffness at the tendon, as already observed for the biceps brachii in people with Parkinson's disease 43, and for the gastrocnemius in patients with spinal cord injury 44,45 and in healthy volunteers 46,47, with conflicting evidence for the lower limb 48. Structural adaptations associated with PSS, e.g., lower MB tension with respect to the tendon 49 and lack of muscle strain during stretch 50, and with limb disuse after stroke 51 can help to support these results. Additionally, soft-tissue mechanical properties may behave differently, depending on joint position during assessment 47,52, which highlights again the importance of measuring different spots within the muscle to characterize PSS 6

       Limitations

      Several limitations need to be acknowledged. First, the subacute group included patients up to 9 months after stroke following previous research on the topic 9. Despite new standards describe chronic as more than 6 months 53, it is also acknowledged that endogenous plasticity persists beyond this period 53, and the chronic stage starts when spontaneous recovery is reduced 9,54. Therefore, one of the main recommendations for stroke research is to report the time from stroke onset 53. Second, there was a wide time range after stroke for participants in the chronic group. Third, it could be argued that the MTS would have been more accurate than the Modified Ashworth scale to screen participants for eligibility 55. However, in the absence of sufficient psychometric evidence to recommend one specific clinical measure 3, the Modified Ashworth scale is easy and quick to complete 13, highly responsive 56, and remains the common tool to quantify spasticity after stroke, despite its limitations 3. Lastly, manual stretch was conducted slowly during evaluation in stretched position to avoid the stretch reflex, although the procedure was not time controlled and possible muscle activation was not monitored by electromyography. Moreover, the time spent in maximum stretch before evaluation was similar for all participants, but it was not standardized.

      Conclusions

      Myotonometry measurements of tone and stiffness can discriminate better between the affected and non-affected sides in people with stroke and between these and healthy controls, when myotonometry is performed with the muscle stretched. Clinical measures of spasticity were not correlated with myotonometry, regardless of the muscle position during evaluation.
      Supplier's list: MyotonPRO: Myoton AS, Lootsa Str. 8A, Tallinn 11415, Estonia.

      Acknowledgement

      We wish to thank all the participants who took part in the study, and the stroke units at CRECER and DACE for helping us during the recruitment process.

      Funding

      This research was partially funded by the Ilustre Colegio Profesional de Fisioterapeutas de Andalucia (grant reference number 03729/19D/MA). The funding source were not involved in the study design, analysis and interpretation of data, or report writing of this study.

      Declaration of interest

      None of the authors has any financial or other interests relating to the manuscript.

      Data availability statement

      The data that support the study findings are available from the corresponding author upon reasonable request.

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