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Evaluation of muscle stiffness in Adhesive Capsulitis with Myoton PRO

Open AccessPublished:September 17, 2022DOI:https://doi.org/10.1016/j.jseint.2022.08.017

      Abstract

      Background

      Adhesive Capsulitis (AC) is characterized by pain and limited range of motion (ROM), caused by stiffness of the joint capsule and coracohumeral ligament. On the other hand, there have been few reports on muscle stiffness in AC. The purpose of this study was to assess muscle stiffness in patients of AC with a portable and non-invasive device, Myoton PRO. We hypothesized that muscle stiffness around shoulder joint increases in AC.

      Methods

      At first, we surveyed correlation between Myoton PRO and shear wave elastography (SWE) with phantoms. Second, reproducibility and repeatability of healthy volunteers with Myoton PRO were evaluated. Finally, muscle stiffness was measured in 40 patients who were diagnosed with AC. Muscle stiffness was quantitatively measured with Myoton PRO. We compared the stiffness of the anterior deltoid (AD), pectoralis major (PM), and latissimus dorsi (LD) in FS patients on both the affected and non-affected sides.

      Results

      Correlation coefficient in SWE and Myoton PRO was 0.99(p=0.001). Reliability of intra- and inter-operator with Myoton PRO was 0.9 or higher. Muscle stiffness values (N/m) of the AD, PM, and LD were 355±61, 252±54, 207±51 in affected sides and 328±50, 252±41, 186±37 in non-affected side, and the differences were significant in the AD and LD (p=0.005, p=0.002, respectively).

      Conclusions

      We used Myoton PRO to evaluate muscle stiffness in FS. The AD and LD muscles of AC patients were significantly stiffer on the affected side compared to the non-affected side.

      Keywords

      Adhesive Capsulitis (AC) is described symptomatically as painful and limited range of motion (ROM) of the shoulder.
      • Neviaser A.S.
      • Neviaser R.J.
      Adhesive Capsulitis of the Shoulder.
      AC occurs in 2% to 5% of the general population.
      • Itoi E.
      • Arce G.
      • Bain G.I.
      • Diercks R.L.
      • Guttmann D.
      • Imhoff A.B.
      • et al.
      Stiffness, 2016 Shoulder Stiffness: Current Concepts and Concerns.
      Limited ROM affects activities of daily living, such as combing hair and washing the body.
      • Magermans D.J.
      • Chadwick E.K.
      • Veeger H.E.
      • van der Helm F.C.
      Requirements for upper extremity motions during activities of daily living.
      The joint capsule and the coracohumeral ligament (CHL) are major factors that contribute to the limited ROM of AC.
      • Cho C.H.
      • Bae K.C.
      • Kim D.H.
      Treatment Strategy for Frozen Shoulder.
      ,
      • Hagiwara Y.
      • Kanazawa K.
      • Ando A.
      • Sekiguchi T.
      • Yabe Y.
      • Takahashi M.
      • et al.
      Clinical outcomes of arthroscopic pan-capsular release with or without entire coracohumeral ligament release for patients with frozen shoulder.
      Moreover, some papers have shown stiffness of the supraspinatus and infraspinatus tendons in AC patients with ultrasound elastography.
      • Wada T.
      • Itoigawa Y.
      • Yoshida K.
      • Kawasaki T.
      • Maruyama Y.
      • Kaneko K.
      Increased Stiffness of Rotator Cuff Tendons in Frozen Shoulder on Shear Wave Elastography.
      ,
      • Yun S.J.
      • Jin W.
      • Cho N.S.
      • Ryu K.N.
      • Yoon Y.C.
      • Cha J.G.
      • et al.
      Shear-Wave and Strain Ultrasound Elastography of the Supraspinatus and Infraspinatus Tendons in Patients with Idiopathic Adhesive Capsulitis of the Shoulder: A Prospective Case-Control Study.
      Although the factors causing limited ROM are important for clinicians and physical therapists to manage the condition, the limited ROM in AC is related to various factors and identifying them can be challenging.
      Recently, Hollmann et al have suggested muscle cause ROM restrictions in AC.
      • Hollmann L.
      • Halaki M.
      • Kamper S.J.
      • Haber M.
      • Ginn K.A.
      Does muscle guarding play a role in range of motion loss in patients with frozen shoulder?.
      In their study, improvements in abduction and external rotation were found under anesthesia compared to preanesthesia in AC. Therefore, the muscle may be an additional mechanism related to the limited ROM in AC. To measure muscle status, shear wave elastography (SWE) has been used for non-invasive and objective measurement.
      • Akagi R.
      • Takahashi H.
      Effect of a 5-week static stretching program on hardness of the gastrocnemius muscle.
      ,
      • Chino K.
      • Takahashi H.
      The association of muscle and tendon elasticity with passive joint stiffness: In vivo measurements using ultrasound shear wave elastography.
      SWE can evaluate the targeted muscle stiffness as Young’s modulus by analyzing shear wave velocity (SWV).
      • Taljanovic M.S.
      • Gimber L.H.
      • Becker G.W.
      • Latt L.D.
      • Klauser A.S.
      • Melville D.M.
      • et al.
      Shear-Wave Elastography: Basic Physics and Musculoskeletal Applications.
      Although SWE is a valid and reliable tool to evaluate muscle stiffness, it is expensive and requires technical expertise to be widely used for research.
      • Feng Y.N.
      • Li Y.P.
      • Liu C.L.
      • Zhang Z.J.
      Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO.
      In contrast, Myoton PRO is a hand-held device and very easy to operate. It can measure muscle stiffness quantitatively and non-invasively like SWE. It is good device to assess superficial skeletal muscle.
      • Liu C.L.
      • Feng Y.N.
      • Zhang H.Q.
      • Li Y.P.
      • Zhu Y.
      • Zhang Z.J.
      Assessing the viscoelastic properties of upper trapezius muscle: Intra- and inter-tester reliability and the effect of shoulder elevation.
      To the best of our knowledge, no clinical studies have reported shoulder muscle measurements in AC with Myoton PRO.
      This study aimed to evaluate the following: 1) correlation between SWE and Myoton PRO; 2) reproducibility and repeatability with Myoton PRO; and 3) muscle stiffness in AC with Myoton PRO. We hypothesized that Myoton PRO is a highly reproducible device that correlates with SWE and that the affected side is stiffer than the non-affected side in AC.

      Methods

      This study was approved by the Tochigi Medical Center Shimotsuga Institutional Review Board (No.129).

      Correlation Myoton PRO and SWE with phantoms

      Before measuring muscle stiffness in AC, we evaluated the correlation between Myoton PRO and SWE using phantoms. There has been no study correlating stiffness in Myoton PRO and SWV in SWE, by using phantoms. We used four different stiffness phantoms (6.0 wt%, 6.5 wt%, 7.0 wt%, and 7.5 wt%) made in Kyoto Kagaku (Kyoto, Japan). The phantoms are water-soluble gel materials made from carboxymethyl cellulose (CMC). The "wt%" indicates the CMC content: the higher the CMC, the stiffer the phantom.

      SWE measurement

      SWE was measured using a Toshiba Aplio i800 ultrasound system equipped with a 5-18 MHz transducer (Canon Medical Systems, Tochigi, Japan). SWE was performed by the same examiner who had more than 5 years of ultrasound experience.

      Myoton PRO measurement

      Myoton PRO (Myoton AS, Tallinn, Estonia) is a handheld device that produces a mechanical impulse on the skin overlying a target structure.
      • Schneebeli A.
      • Falla D.
      • Clijsen R.
      • Barbero M.
      Myotonometry for the evaluation of Achilles tendon mechanical properties: a reliability and construct validity study.
      The measurement method applied by Myoton PRO involves a mechanical impact that is released under a constant pre-pressure (0.18 N) on the subcutaneous panniculus above the muscle or tendon being measured. The oscillation of the tissue under the probe enables the calculation of the viscoelastic properties of the tissue. One parameter is dynamic stiffness, which has been used to identify muscle character.
      • Schneider S.
      • Peipsi A.
      • Stokes M.
      • Knicker A.
      • Abeln V.
      Feasibility of monitoring muscle health in microgravity environments using Myoton technology.
      The stiffness value can be calculated as the maximum acceleration of the oscillation and deformation of the tissue detected by the transducer (N/m).
      • Chen G.
      • Wu J.
      • Chen G.
      • Lu Y.
      • Ren W.
      • Xu W.
      • et al.
      Reliability of a portable device for quantifying tone and stiffness of quadriceps femoris and patellar tendon at different knee flexion angles.
      We obtained measurements three times with Myoton PRO and SWE, assessed the average of the three times, and evaluated the correlation of SWV with SWE, and of stiffness with Myoton PRO.

      Reproducibility and repeatability with Myoton PRO

      To evaluate the intra- and inter-observer repeatability with Myoton PRO, ten healthy volunteers(HV)were measured (8 men and 2 women with a mean age of 32.2 ± 9.7 years). Myoton PRO measures the stiffness of the superficial muscles. Therefore, we selected the anterior deltoid (AD), pectoralis major (PM), and latissimus dorsi (LD). The AD limits extension of the shoulder joint, the PM limits shoulder abduction, the LD limits shoulder flexion, and the AD, PM, and LD are important for movement of the shoulder joint.
      Measurement locations were determined using bony landmarks, as shown in Figure 1. All measurements were performed in the supine position. The AD was measured at the midpoint between the clavicle and the rough surface of the deltoid muscle. The PM was measured at three-quarters of the line connecting the sternum and the ridge of the nodule. The LD was measured at a point 5 cm above the lower angle of the scapula with the shoulder flexed at 80°. Examiner 1 performed two sets of measurements spaced 15 min apart to determine the intra-rater reliability. Examiner 2 performed the measurements during the first examiner’s first and second sets.
      Figure thumbnail gr1
      Figure 1Measurement of each muscle. (A) The anterior deltoid was measured at the midpoint between the clavicle and the rough surface of the deltoid muscle. (B)The pec major was measured at three-quarters of the line connecting the sternum and the ridge of the nodule. (C) The latissimus dorsi was measured at a point 5 cm above the lower angle of the scapula with the shoulder flexed at 90°.

      Evaluation of muscle stiffness in AC

      This was a cross-sectional observational study. The subjects were 95 patients who were diagnosed with AC at our hospital between September 2019 and December 2020. According to previous studies, the limitations of ROM in AC were defined as those of <100° in forward flexion, <10° in external rotation, and <L5 level in internal rotation.
      • Itoi E.
      • Arce G.
      • Bain G.I.
      • Diercks R.L.
      • Guttmann D.
      • Imhoff A.B.
      • et al.
      Stiffness, 2016 Shoulder Stiffness: Current Concepts and Concerns.
      The inclusion criteria included those patients who were diagnosed with AC at the time of the study. The exclusion criteria were: diabetes (25 patients), AC without contracture that defined the previous studies (24 patients), post-breast cancer surgery (3 patients), bilaterally symptomatic (2 patients), and calcific tendinitis (1 patient). After applying the exclusion criteria, 40 patients were finally selected. All patients underwent physical examination and imaging studies, including radiography and magnetic resonance imaging (MRI). We examined muscle stiffness in AC on the AD, PM, and LD of both the affected and non-affected sides using Myoton PRO. It was measured twice for each muscle and analyzed using average values.

      Statistical analysis

      To investigate the relationship between the stiffness values determined using Myoton PRO and the SWV obtained by SWE, Pearson correlation coefficients were calculated for each phantom. Additionally, linear regression analysis was performed for the stiffness and SWV.
      To evaluate the intra- and inter-operator reliability of the HV, the intraclass correlation coefficient (ICC) was used. The reliability evaluation standard was judged to be high when the ICC was 0.75 or higher.
      • Enderlein G.
      • Fleiss J.L.
      The Design and Analysis of Clinical Experiments. Wiley, New York – Chichester – Brislane – Toronto – Singapore.
      To evaluate muscle stiffness in AC patients, the detection power required for the paired t-test (effect size = 0.25 [medium], α error = .05) was calculated using G * Power 3.1 software (Heinrich Heine University, Düsseldorf, Germany). In this study, the detection power was 0.87 for 40 participants. For continuous variables, statistical analysis was performed using the t-test for all AC patients and the independent t-test for gender-separated cases. For categorical variables, we used the χ2 test or Fisher's exact test. The level of statistical significance was set at p<0.05. Calculations were performed using SPSS 25 software (IBM, Armonk, NY, USA).

      Results

      Correlation of SWE and Myoton PRO with four phantoms

      In the 6.0 wt% phantom, SWV was 2.76±0.01 m/s and stiffness was 130.3±0.5 N/m. In the 6.5 wt% phantom, SWV was 2.89±0.03 m/s and stiffness was 137.3±0.5 N/m. In the 7.0 wt% phantom, SWV was 3.01±0.02 m/s and stiffness was 147.3±0.9 N/m. In the 7.5 wt% phantom, SWV was 3.34±0.03 m/s and stiffness was 163.3±0.5 N/m. Correlation coefficient for SWV in SWE and stiffness in Myoton PRO was 0.99 (P<0.001) (Figure 2).
      Figure thumbnail gr2
      Figure 2Results of correlation between SWV and stiffness Correlation coefficient for SWV in SWE and stiffness in Myoton PRO was 0.99 (P<0.001).

      Reproducibility and repeatability in HV with Myoton PRO

      The details are listed in Table 1. In the AD, PM, and LD muscles on both the dominant and non-dominant sides, the intra- and inter-operator was 0.9 or higher. There was no significant difference in muscle stiffness between the dominant and non-dominant sides in any muscle (Table 2).
      Table 1Intra- and inter-rater reliability for Evaluator 1 and Evaluator 2 for
      parameters in healthy volunteers
      Evaluator 1Evaluator 2intra-inter-
      trial 1trial 2trial 3operator95%CIoperator95%CI
      DominantAD291±36295±37299±370.950.83-0.990.940.77-0.98
      sidePM212±42214±46218±460.980.94-1.000.980.90-0.99
      LD204±29201±30204±320.970.90-0.990.960.86-0.99
      Non-AD294±47293±49284±400.970.90-0.990.930.69-0.98
      dominantPM219±39217±37218±410.940.80-0.990.940.77-0.99
      sideLD184±44183±48185±410.990.96-0.990.940.78-0.99
      AD, anterior deltoid; PM, pec major; LD, latissimus dorsi; CI, confidence interval
      Data are presented as means ± standard deviation
      Table 2Comparison dominant side and non-dominant side for muscle stiffness in healthy volunteers
      (n=10)DominantNon-dominantP value
      AD293 ± 36294 ±480.94
      PM213 ± 44218 ± 370.51
      LD202 ± 29181 ± 420.10
      AD, anterior deltoid; PM, pec major; LD, latissimus dorsi
      Data are presented as means ± standard deviation

      Comparison of stiffness between the affected side and non-affected side using Myoton PRO

      The demographic and clinical data are shown in Table 3. We found significant differences in AD and LD muscle stiffness in AC (Table 4). The PM muscle showed no difference in AC.
      Table 3Demographic and clinical data in AC patients
      Variables (n=40)
       Age56.9 ± 8.4
      Gender (female / male)30 / 10
      Height(cm) / Weight(kg)164 ± 19.3 / 59.4 ± 10.6
      Affected side
       Dominant side / Non-dominant side15 /25
      Duration of symptoms6.2 ± 2.8
      NRS score at motion8.4 ± 2.6
      Range of motion (degrees)
       Forward flexion85 ±12
       Abduction63 ± 15
       External rotation at side3 ± 8
       Internal rotationButtock (Buttock-Sacrum)
      Constant score25 ± 5
      ASES score27 ± 15
      AC, Adhesive Capsulitis; NRS, numerical rating scale; ASES, American Shoulder and Elbow Surgery
      Data are presented as means ± standard deviation
      Table 4Stiffness values in AC patients
      Variables(n=40)Non-affected sideAffected sideP value
      AD328 ± 50355 ± 61< 0.01
      PM252 ± 41252 ± 540.98
      LD186 ± 37207 ± 51< 0.01
      AD, anterior deltoid; PM, pec major; LD, latissimus dorsi
      Data are presented as means ± standard deviation

      Discussion

      In this study, we found that Myoton PRO is a highly reproducible device that correlates with SWE. Additionally, it was shown that the AD and LD muscles on the affected side were stiffer than those in the non-affected side in AC.
      At first, we indicated Myoton PRO and SWE were significantly correlated on using phantoms. Feng et al reported the moderate correlation between the two devices in the gastrocnemius and Achilles tendons of healthy adults.
      • Feng Y.N.
      • Li Y.P.
      • Liu C.L.
      • Zhang Z.J.
      Assessing the elastic properties of skeletal muscle and tendon using shearwave ultrasound elastography and MyotonPRO.
      In addition, Kerry et al presented the low to moderate correlation between the two devices in three types of muscle contraction in the infraspinatus, erector spinae, and gastrocnemius muscles.

      Kelly J P, Koppenhaver SL, Michener LA, Proulx L, Bisagni F, Cleland JA. Characterization of tissue stiffness of the infraspinatus, erector spinae, and

      We investigated the correlation between the SWE and Myoton PRO using phantoms which is not anisotropic like muscles. Consequently, our result of correlation coefficient might be higher (≥0.9) compared to those of other papers.
      As a second study, we showed that intra-and inter-rater reliabilities with Myoton PRO were very high. Yeo et al evaluated muscle stiffness of PM in patients with breast cancer by Myoton PRO.
      • Yeo S.M.
      • Kang H.
      • An S.
      • Cheong I.
      • Kim Y.
      • Hwang J.H.
      Mechanical Properties of Muscles around the Shoulder in Breast Cancer Patients: Intra-rater and Inter-rater Reliability of the MyotonPRO.
      They presented both intra-rater and inter-rater reliability were high. There are no reports on AD and LD muscle stiffness measured by Myoton PRO. This is the first paper surveying muscle stiffness of the AD and LD and the reproducibility when using Myoton PRO for them.
      Although our result indicated that the AD and LD muscles on the affected side were stiffer than those on the non-affected side in AC, there have been few studies on muscle stiffness in AC. Wada et al reported, using SWE, that the SSP tendon, ISP tendon, and CHL were stiff, however they did not observe muscle stiffness around the shoulder.
      • Wada T.
      • Itoigawa Y.
      • Yoshida K.
      • Kawasaki T.
      • Maruyama Y.
      • Kaneko K.
      Increased Stiffness of Rotator Cuff Tendons in Frozen Shoulder on Shear Wave Elastography.
      Hollman et al reported that improvements of shoulder ROM under anesthesia in AC may be due to pain avoidance or pain-related cognition.
      • Hollmann L.
      • Halaki M.
      • Kamper S.J.
      • Haber M.
      • Ginn K.A.
      Does muscle guarding play a role in range of motion loss in patients with frozen shoulder?.
      This behavior often results in motor adaptations such as muscle protection and reduced ROM.
      • Matheve T.
      • Liesbet D.B.
      • Bogaerts K.
      • Timmermans A.
      Lumbar range of motion in chronic low back pain is predicted by task-specific, but not by general measures of pain-related fear.
      In this research, the pain level of the subjects scored NRS was higher than in previous papers; therefore, pain might have influenced greater to muscle stiffness.
      • Wada T.
      • Itoigawa Y.
      • Yoshida K.
      • Kawasaki T.
      • Maruyama Y.
      • Kaneko K.
      Increased Stiffness of Rotator Cuff Tendons in Frozen Shoulder on Shear Wave Elastography.
      According to our outcomes, we presented that the AD and LD muscles were stiffer in the affected side than in the non-affected side and the PM muscle was not significantly different in those. The reason for this was thought to be that the muscles of the AD and LD muscles were in the stretched position, while the PM muscles were in the resting position, so that the stretch stimulation might affect the muscle stiffness. In the future, it may be needed to measure the muscle stiffness at different limb position.
      There were several limitations to our study. First, the muscles measured by Myoton PRO were specific. Considering the kinematics of the shoulder joint, it is important to evaluate the rotator cuff muscles. However, this study targeted only the surface muscles because Myoton PRO can measure only the surface layer. Second, the measurement was performed in the supine position in consideration of the effect not to increase pain. Therefore, only the parts that could be measured in that position could be observed. Third, Myoton PRO cannot evaluate muscles alone. Skin stiffness or subcutaneous fat thickness may also affect the measuring result. It is considered that the subjects who have skin disease or be severe obesity are not adapted to this device. Myoton PRO has some weak points. However, it may be a reproducible and useful device to measure muscle stiffness if you understand the properties. Lastly, this study suggested only phenomenon of muscle stiffness in AC. The correlation between clinical symptoms and Myoton PRO measurements is unclear. Our result did not explain clinical significance enough, so in the future we need to investigate the impact of therapeutic intervention to stiff muscle in AC.

      Conclusions

      Myoton PRO may be a helpful device to evaluate muscle stiffness in a specific part. In AC, there was significant stiffness in the AD and LD. In addition to the joint capsule and CHL, stiffness of the AD and LD could warrant further exploration in regard to their role in management of AC.

      Acknowledgment

      We thank Leonie McKinlay, DVM, from Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

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