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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

      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 patients with stroke. 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, 31 controls) were recruited (N=71).

      Intervention

      Muscle mechanical properties were measured bilaterally with a MyotonPRO at muscle belly and musculotendinous sites during 2 protocols (muscle relaxed or in maximal bearable stretched position).

      Main Outcome Measures

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

      Results

      The analysis of variance 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 nonspastic sides, but only at the biceps brachii. Overall, there was a significant increase in tone and stiffness in the chronic stroke group and in myotendinous sites compared with muscle belly sites (all, P<.05). No correlations were found between myotonometry and the MTS.

      Conclusions

      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 (poststroke spasticity)
      Spasticity is a frequent and disabling poststroke sequela, with an estimated prevalence of 25%.
      • Zeng H
      • Chen J
      • Guo Y
      • Tan S.
      Prevalence and risk factors for spasticity after stroke: a systematic review and meta-analysis.
      Despite being a well-known disorder, there is little consensus on how to measure spasticity.
      • Lehoux MC
      • Sobczak S
      • Cloutier F
      • Charest S
      • Bertrand-Grenier A.
      Shear wave elastography potential to characterize spastic muscles in stroke survivors: literature review.
      Subjective scales are common in the clinical setting, with limited evidence to support their use because they lack proper validity,
      • Aloraini SM
      • Gäverth J
      • Yeung E
      • MacKay-Lyons M.
      Assessment of spasticity after stroke using clinical measures: a systematic review.
      reliability, and reproducibility.
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      Clinical measures cannot discriminate between the neural and nonneural (peripheral) components of spasticity,
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      except the Modified Tardieu Scale (MTS). The peripheral contribution to poststroke spasticity (PSS) can be quantified for clinical and research purposes using objective, noninvasive methods, for example, shear-wave elastography and myotonometry.
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      ,
      • Tran A
      • Gao J.
      Quantitative ultrasound to assess skeletal muscles in post stroke spasticity.
      Myotonometry represents a valid, reliable, and convenient tool
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      ,
      • 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.
      that has proven to be useful to monitor PSS after conservative or invasive treatments.
      • Megna M
      • Marvulli R
      • Farì G
      • et al.
      Pain and muscles properties modifications after botulinum toxin type A (BTX-A) and radial extracorporeal shock wave (rESWT) combined treatment.
      However, current evidence on the ability of myotonometry to discriminate between spastic and nonspastic muscles after stroke is scarce and conflicting.
      • 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.
      It has been recommended to conduct myotonometry measurement of PSS at several muscle sites of testing and in different muscle positions, that is, relaxed or stretched,
      • 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.
      to get a clear picture of how muscle mechanical properties may change after stroke
      • Burridge JH
      • Wood DE
      • Hermens HJ
      • et al.
      Theoretical and methodological considerations in the measurement of spasticity.
      and in response to rehabilitation programs.
      This study aimed to investigate the differences in myotonometry scores for muscle tone and stiffness in patients with stroke, comparing sides (affected vs nonaffected), sites (muscle belly [MB] vs musculotendinous [MT]), and groups (subacute stroke, chronic stroke, control), during 2 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 nonaffected sides in patients with stroke and between individuals with or without stroke.

      Methods

      Design

      We conducted a multicenter, cross-sectional study, including adults with subacute (6-36 weeks after the event)
      • 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.
      or chronic (more than 36 weeks) stroke
      • 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.
      and participants without stroke. 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 Strengthening the Reporting of Observational Studies in Epidemiology 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,
      • 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.
      which addresses the involuntary muscle activation feature of spasticity
      • 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.
      as the resistance to a passive movement.
      • Bohannon R
      • Smith M.
      Interrater reliability of a Modified Ashworth Scale of muscle spasticity.
      The exclusion criteria were as follows: cognitive impairtment (score >24 in the Mini-Mental State Examination),
      • Quinn TJ
      • Elliott E
      • Langhorne P.
      Cognitive and mood assessment tools for use in stroke.
      diagnosed mood disorder or other neurologic condition, prior severe upper or lower limb trauma, changes in medication for PSS in the previous 48 hours, treatment with botulinum toxin injections within 12 weeks or during the study period, and an epileptic crisis during the previous week. Those in the control group without stroke 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.
      • 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.
      ,a The device contains a probe that applies an initial load of 0.18 N to the skin and then adds up consecutive short impulses (0.40N) to the subcutaneous tissue to characterize mechanical properties. The MyotonPRO calculates muscle tone (tension) by measuring the natural frequency of the acceleration signal and muscle stiffness by measuring the damped natural oscillation response, using an accelerometer.
      • 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.
      Measurements were taken bilaterally at MB and MT sites, with the muscle relaxed or in the maximum bearable stretched position. The mean score of the 2 consecutive 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 measuring the gastrocnemius, participants lied in prone with approximately 45° of knee flexion. Three sites of muscle testing were included, namely 1 MT location and 2 MB sites. For MB, the mean value at the 2 sites was used in the analysis.
      The level of PSS was measured with the MTS,
      • 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.
      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.b At V3, the quality of muscle reaction was scored from 0-5, where 0 represents no resistance during passive motion and 5 represents that the joint cannot be moved.
      • Petek Balci B
      Spasticity measurement.
      To conduct the MTS at the biceps brachii, participants were supine, and the elbow was initially positioned in maximal flexion and supination. For the lower limb, participants remained prone with knees fully extended and feet outside the table.
      All outcomes were collected by the same examiner, who had more than 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.c We assumed an α level of 0.05, 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 version 26.0.d Normal distribution of the data were evaluated with the Shapiro-Wilk test. We used a mixed-model analysis of variance to compare differences in tone and stiffness of the biceps brachii and gastrocnemius, using muscle position (relaxed vs stretched), side (affected vs nonaffected), and site (MB vs MT) as the within-participant factors and group (subacute stroke, chronic stroke, controls) as the between-participant factor. The Spearman 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<.05.

      Data availability

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

      Results

      Seventy-one participants (20 subacute stroke, 20 chronic stroke, 31 controls) were recruited (fig 1). The clinical and demographic characteristics of the sample are listed in table 1.
      Fig 1
      Fig 1Flowchart diagram of the study participants.
      Table 1Baseline clinical and demographic features of participants
      CharacteristicSubacute Stroke (n=20)Chronic Stroke (n=20)Control Group (n=31)P Value
      Age (y), mean ± SD60.2±9.761.45±9.760.8±10.6.926
      Sex (female), n, (%)7 (35)7 (35)14 (45.2).689
      Time after stroke (wk), median (IQR)17 (6-34)242.5 (58-1108)NA<.001
      Affected side, left, n (%)11 (55)15 (75)NA.289
      Hand dominance (right; left; ambidextrous), n (%)20 (100)17 (85); 1 (5); 2 (10)25 (80.6); 6 (19.4).131
      Leg dominance (right;

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

      1 (5)
      16 (80);

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

      5 (16.1)
      .319
      Abbreviation: NA, Not applicable.

      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 analysis of variance revealed a significant effect of muscle position during myotonometry assessment (relaxed vs stretched) on muscle mechanical properties for (1) the biceps brachii: tone, F=59.567, P<.001, η2=0.095; stiffness, F=22.808, P<.001, η2=0.039 and (2) the gastrocnemius: tone, F=313.2, P<.001; η2=0.365; stiffness: F=341.57; P<.001; η2=0.386. 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 2 measurement protocols
      MeasurementSubacute Stroke GroupChronic Stroke GroupControl Group
      SideMuscle PositionToneStiffnessToneStiffnessToneStiffness
      MB sitesDominant/nonaffectedRelaxed

      Stretched
      14.2±1.8

      15.0±1.9
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      259.1±53.3

      267.6±50.7
      14.8±1.5

      15.3±1.9
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      271.6±40.7

      276.4±44.8
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      14.7±2.1

      15.7±2.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      271.2±48.7

      289.3±53.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      Nondominant/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
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      301.5±60.2

      315.9±68.3
      14.6±1.8

      15.6±2.0
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      276.3±44.6

      291.9±43.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      MT sitesDominant/nonaffectedRelaxed

      Stretched
      14.3±1.3

      16.4±1.8
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      245.6±33.2

      285.3±48.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      15.1±2.9

      16.4±2.3
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      275.7±75.2

      290.7±51.8
      14.3±1.5

      16.2±1.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      253.4±39.7

      282.41±36.0
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      Nondominant/affectedRelaxed

      Stretched
      14.4±2.5

      16.2±2.3
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      251.9±54.2

      285.3±62.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      14.2±1.7

      16.3±2.5
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      259.9±39.1

      307.9±58.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      14.5±1.9

      16.3±2.1
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      258.4±48.4

      288.4±50.1
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      low asterisk Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      Table 3Muscle tone (Hz) and stiffness (N/m) for the gastrocnemius at the different sites, sides, and groups during the 2 measurement protocols
      MeasurementSubacute Stroke GroupChronic Stroke GroupControl Group
      SideMuscle PositionToneStiffnessToneStiffnessToneStiffness
      MB sitesDominant/nonaffectedRelaxed

      Stretched
      14.8±1.3

      18.8±2.6
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      281.8±28.7

      348.4±50.8
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      16.4±1.9

      20.1±3.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      291.8±35.8

      387.9±93.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      15.3±1.1

      19.8±2.2
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      285.6±18.1

      383.3±65.2
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      Nondominant/affectedRelaxed

      Stretched
      15.1±1.9

      19.0±3.1
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      283.3±24.7

      350.2±56.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      16.7±2.9

      19.7±3.3
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      321.0±58.2

      386.6±106.2
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      15.6±1.4

      19.8±2.5
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      286.2±21.4

      375.4±64.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      MT sitesDominant/nonaffectedRelaxed

      Stretched
      21.9±2.4

      26.8±4.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      442.2±56.3

      594.6±123.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      22.8±4.0

      27.6±3.1
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      468.5±94.5

      620.1±103.4
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      23.9±3.3

      30.3±4.6
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      483.2±58.6

      697.6±128.5
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      Nondominant/affectedRelaxed

      Stretched
      21.8±2.9

      27.0±4.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      433.3±63.9

      577.6±132.8
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      23.0±3.1

      27.1±3.3
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      459.4±75.9

      599.2±104.2
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      23.5±2.6

      28.9±3.7
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      482.5±56.5

      659.8±113.5
      Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).
      low asterisk Significant differences in the within-groups analysis when comparing scores at the same site and side between the 2 different protocols (muscle relaxed vs stretched).

      Discriminative ability between spastic and nonspastic muscles

      Myotonometry measurements in relaxed position could not discriminate between the affected and nonaffected sides or between patients with stroke and controls (all, P>.05), except for the lower limb, where higher values were found in the chronic stroke and control groups compared with 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 (1) higher biceps brachii stiffness in the chronic stroke than in the control group (P=.045) and (2) lower gastrocnemius tone and stiffness in participants with subacute stroke compared with controls without stroke (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 (1) the biceps brachii: tone, F=8.158, P<.004, η2=0.015; stiffness, F=6.330, P<.012, η2=0.012 and (2) the gastrocnemius: tone, F=6.089, P<.014, η2=0.011; stiffness: F=39.847, P<.001, η2=.068. Differences between sites of testing were found in the 2 protocols, with higher tone and stiffness at MT sites than 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
      MeasureSubacute 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
      Abbreviations: V1, joint angle at slow passive stretch (degrees); V3, “catch angle” at fast passive stretch (degrees); X, quality of muscle reaction at V3, from 0-5.

      Discussion

      The present findings partly agree with our hypotheses. Tone and stiffness values changed among the 2 protocols, and myotonometry measurements with the muscle stretched could discriminate between the spastic and nonspastic 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.
      • Puce L
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      • Marinelli L
      • et al.
      Clinical neurophysiology practice spasticity, spastic dystonia, and static stretch reflex in hypertonic muscles of patients with multiple sclerosis.

      Comparison between measurement protocols

      Myotonometry is a valid and easy-to-use approach to objectively quantify muscle mechanical properties in people after stroke.
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      ,
      • 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.
      However, its high environmental sensitivity
      • Luo Z
      • Lo WLA
      • Bian R
      • Wong S
      • Li L.
      Advanced quantitative estimation methods for spasticity: a literature review.
      and the large within- and between-participants variability
      • Eby SF
      • Zhao H
      • Song P
      • et al.
      Quantifying spasticity in individual muscles using shear wave elastography.
      together with assessment-related aspects, such as muscle position and operator's experience,
      • Luo Z
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      Advanced quantitative estimation methods for spasticity: a literature review.
      ,
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      Sharp changes in muscle tone in humans under simulated microgravity.
      stress the importance of agreeing on a standardized evaluation protocol.
      Most previous research in patients with stroke 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.
      • Xiaoyan L
      • Shin H
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      • Li S
      • Zhou P.
      Assessing muscle compliance in stroke with the myotonometer.
      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,
      • Condliffe EG
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      • Patten C.
      Reliability of elbow stretch reflex assessment in chronic post-stroke hemiparesis.
      which may become more evident with the muscle stretched than relaxed.
      • Gao J
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      • et al.
      Quantitative ultrasound imaging to assess the biceps brachii muscle in chronic post-stroke spasticity: preliminary observation.
      PSS is also related with shorter muscle fascicles and more compliant tendons that do not respond properly to stretch, increasing tone and stiffness.
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      • Barber L
      • et al.
      The mechanisms of adaptation for muscle fascicle length changes with exercise: implications for spastic muscle.
      Additionally, thixotropy, as the influence of movement and time of recovery after movement on mechanical properties,
      • Lakie M
      • Campbell KS.
      Muscle thixotropy—where are we now?.
      is altered after stroke
      • Vattanasilp W
      • Ada L
      • Crosbie J.
      Contribution of thixotropy, spasticity, and contracture to ankle stiffness after stroke.
      and can modify muscle stiffness
      • Lakie M
      • Campbell KS.
      Muscle thixotropy—where are we now?.
      and contribute to intrinsic hypertonia.
      • Bakheit AMO.
      The pharmacological management of post-stroke muscle spasticity.
      All in all, changes in mechanical properties after stroke are linked to changes in muscle morphology and composition.
      • Lieber RL
      • Ward SR.
      Cellular mechanisms of tissue fibrosis. 4. Structural and functional consequences of skeletal muscle fibrosis.
      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
      • Xiaoyan L
      • Shin H
      • Zong Y
      • Li S
      • Zhou P.
      Assessing muscle compliance in stroke with the myotonometer.
      but in contradiction with studies that used myotonometry with the muscle contracted.
      • Leonard CT
      • Stephens JU
      • Stroppel SL.
      Assessing the spastic condition of individuals with upper motoneuron involvement: validity of the myotonometer.
      ,
      • Rydahl SJ
      • Brouwer BJ.
      Ankle stiffness and tissue compliance in stroke survivors: a validation of myotonometer measurements.
      The scarce and contradictory literature on this issue, as well as the differences among studies in myotonometry devices and muscle position, can account for the lack of agreement.

      Discriminative ability between spastic and nonspastic muscles

      In patients with stroke, myotonometry could only discriminate between sides with the muscle stretched and at the upper limb. In agreement with most literature on the topic,
      • Xiaoyan L
      • Shin H
      • Zong Y
      • Li S
      • Zhou P.
      Assessing muscle compliance in stroke with the myotonometer.
      ,
      • Li X
      • Shin H
      • Li S
      • Zhou P.
      Assessing muscle spasticity with myotonometric and passive stretch measurements: validity of the myotonometer.
      • Leng Y
      • Lo WLA
      • Hu C
      • et al.
      The effects of extracorporeal shock wave therapy on spastic muscle of the wrist joint in stroke survivors: evidence from neuromechanical analysis.
      • 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.
      we observed higher stiffness at the spastic biceps brachii than the nonspastic side. It has been argued that stretching of the biceps brachii evokes higher resistance to elbow extension,
      • Gao J
      • He W
      • Du LJ
      • et al.
      Quantitative ultrasound imaging to assess the biceps brachii muscle in chronic post-stroke spasticity: preliminary observation.
      and this can make the muscle stiffer and increase tone.
      • Wu CH
      • Ho YC
      • Hsiao MY.
      Evaluation of post-stroke spastic muscle stiffness using shear wave ultrasound elastography.
      ,
      • Haugh A
      • Pandyan A
      • Johnson G.
      A systematic review of the Tardieu Scale for the measurement of spasticity.
      Nonetheless, evidence on this issue is still preliminary and inconsistent.
      • Chuang LL
      • Wu CY
      • Lin KC.
      Reliability, validity, and responsiveness of myotonometric measurement of muscle tone, elasticity, and stiffness in patients with stroke.
      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
      • 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.
      ,
      • 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.
      • Wang JS
      • Lee SB
      • Moon SH.
      The immediate effect of PNF pattern on muscle tone and muscle stiffness in chronic stroke patient.
      • 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.
      in individuals with acute
      • 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.
      or chronic stroke.
      • 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.
      ,
      • 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.
      ,
      • Wang JS
      • Lee SB
      • Moon SH.
      The immediate effect of PNF pattern on muscle tone and muscle stiffness in chronic stroke patient.
      Bilateral adaptations of the lower limbs, especially in those who remain nonphysically active after stroke,
      • 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.
      could explain the lack of discriminative ability at the gastrocnemius.
      Regarding the comparison between spastic and control group muscles, higher tone and stiffness are often expected in chronic poststroke stages,
      • 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.
      ,
      • Wang JS
      • Lee SB
      • Moon SH.
      The immediate effect of PNF pattern on muscle tone and muscle stiffness in chronic stroke patient.
      although the changes in mechanical properties seem to depend on the assessed muscles.
      • 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.
      ,
      • Wang JS
      • Lee SB
      • Moon SH.
      The immediate effect of PNF pattern on muscle tone and muscle stiffness in chronic stroke patient.
      As in the present study, biceps brachii tone and stiffness have shown to be increased in patients with chronic stroke.
      • Gao J
      • He W
      • Du LJ
      • et al.
      Quantitative ultrasound imaging to assess the biceps brachii muscle in chronic post-stroke spasticity: preliminary observation.
      ,
      • Lee S
      • Spear S
      • Rymer W.
      Quantifying changes in material properties of stroke-impaired muscle.
      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.
      • Mirbagheri MM
      • Tsao C
      • Rymer WZ.
      Natural history of neuromuscular properties after stroke: a longitudinal study.
      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.
      • 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.

      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 toward higher tone and stiffness at the tendon, as already observed for the biceps brachii in people with Parkinson disease
      • 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.
      and for the gastrocnemius in patients with spinal cord injury
      • Ge JS
      • Chang TT
      • Zhang ZJ.
      Reliability of myotonometric measurement of stiffness in patients with spinal cord injury.
      ,
      • Ko CY
      • Choi HJ
      • 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.
      and in healthy volunteers,
      • Feng YN
      • Li YP
      • Liu CL
      • Zhang ZJ.
      Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO.
      ,
      • Huang J
      • Qin K
      • Tang C
      • 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.
      with conflicting evidence for the lower limb.
      • 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.
      Structural adaptations associated with PSS, for example, lower MB tension with respect to the tendon
      • Faturi FM
      • Lopes Santos G
      • Ocamoto GN
      • Russo TL
      Structural muscular adaptations in upper limb after stroke: a systematic review.
      and lack of muscle strain during stretch
      • Chardon MK
      • Suresh NL
      • Dhaher YY
      • Rymer WZ.
      In-vivo study of passive musculotendon mechanics in chronic hemispheric stroke survivors.
      and with limb disuse after stroke
      • Narici MV
      • Maganaris CN.
      Plasticity of the muscle-tendon complex with disuse and aging.
      can help to support these results. Additionally, soft tissue mechanical properties may behave differently, depending on joint position during assessment,
      • Huang J
      • Qin K
      • Tang C
      • 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.
      ,
      • 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.
      which highlights again the importance of measuring different spots within the muscle to characterize PSS.
      • 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.

      Study limitations

      Several limitations need to be acknowledged. First, the subacute group included patients up to 9 months after stroke, in accordance with previous research on the topic.
      • 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.
      Despite new standards describing chronic as more than 6 months,
      • Bernhardt J
      • Hayward KS
      • Kwakkel G
      • et al.
      Agreed definitions and a shared vision for new standards in stroke recovery research: the Stroke Recovery and Rehabilitation Roundtable taskforce.
      endogenous plasticity persists beyond this period,
      • Bernhardt J
      • Hayward KS
      • Kwakkel G
      • et al.
      Agreed definitions and a shared vision for new standards in stroke recovery research: the Stroke Recovery and Rehabilitation Roundtable taskforce.
      and the chronic stage starts when spontaneous recovery is reduced.
      • 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.
      ,
      • Nichols-Larsen DS
      • Clark PC
      • Zeringue A
      • Greenspan A
      • Blanton S.
      Factors influencing stroke survivors’ quality of life during subacute recovery.
      Therefore, one of the main recommendations for stroke research is to report the time from stroke onset.
      • Bernhardt J
      • Hayward KS
      • Kwakkel G
      • et al.
      Agreed definitions and a shared vision for new standards in stroke recovery research: the Stroke Recovery and Rehabilitation Roundtable taskforce.
      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.
      • Patrick E
      • Ada L
      The Tardieu Scale differentiates contracture from spasticity whereas the Ashworts Scale is confounded by it.
      However, in the absence of sufficient psychometric evidence to recommend 1 specific clinical measure,
      • Aloraini SM
      • Gäverth J
      • Yeung E
      • MacKay-Lyons M.
      Assessment of spasticity after stroke using clinical measures: a systematic review.
      the Modified Ashworth Scale is easy and quick to complete,
      • Bohannon R
      • Smith M.
      Interrater reliability of a Modified Ashworth Scale of muscle spasticity.
      is highly responsive,
      • Chen CL
      • Chen CY
      • Chen HC
      • et al.
      Responsiveness and minimal clinically important difference of Modified Ashworth Scale in patients with stroke.
      and remains the common tool to quantify spasticity after stroke, despite its limitations.
      • Aloraini SM
      • Gäverth J
      • Yeung E
      • MacKay-Lyons M.
      Assessment of spasticity after stroke using clinical measures: a systematic review.
      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 nonaffected sides in people with stroke and between these and controls without stroke when myotonometry is performed with the muscle stretched. Clinical measures of spasticity were not correlated with myotonometry, regardless of the muscle position during evaluation.

      Suppliers

      a. MyotonPRO; Myoton AS.
      b. Electrogoniometer; Biometrics Ltd.
      c. G*Power software v. 3.1.9.2; Heinrich-Heine University.
      d. PASW Advanced Statistics version 26.0; SPSS Inc.

      Acknowledgments

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

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