MyotonPRO is a reliable and repeatable tool for measuring mechanical properties of the upper limp muscles in patients with chronic stroke

The purpose of the present study was to investigate the inter-rater and intra-rater reliability of the MyotonPRO for measuring the mechanical properties of the upper limp muscles in patients with chronic stroke. The study was conducted with 20 stroke patients (14 males, 6 females) with age range of 36–84 years (65.1 ± 11.2 years). The oscillation frequency, stiffness, and logarithmic decrement of the biceps brachii, triceps brachii, deltoid, and upper trapezius muscles were measured using a MyotonPRO (Muomeetria Ltd., Tallinn, Estonia). The measurements were conducted by two physiotherapists to determine the inter-rater reliability of the device. A physiotherapist repeated the measurements 3 days after the rst measurements for determining the intra-rater reliability of the device. The ICCs of the all assessed muscles ranged between 0.72 and 0.97. The coecient of variation of all muscles ranged within 3.2%-11.0%, from 3.4–9.7% for oscillation frequency, from 3.9–7.4% for stiffness, and from 3.2– 11.0% for decrement. The standard error of measurement in the assessed muscles ranged from 0.5 to 1.2 Hz for frequency, from 9.2 to 21.2 N/m for stiffness, and from 0.1 to 0.4 for decrement. The results obtained show that MyotonPRO has a good to excellent intra-rater and inter-rater reliability for measuring the tone, stiffness, and elasticity of the deltoid, biceps brachii, triceps brachii, and upper trapezius muscles in patients with chronic stroke. MyotonPRO can be used for the diagnostic and therapeutic intention in patients with chronic stroke.


Introduction
Stroke is a general health problem worldwide, and it is one of the major causes of disability in adults 1,2 .
One of the most common de cits after stroke is upper limb impairment, which can cause functional limitations in daily life activities 3,4 . Upper limb impairment in stroke patients is associated with impaired detection of sensory information and disturbed performance of motor tasks 5 . One of the most prevalent causes of the disturbed performance of motor tasks following stroke is changes in muscle mechanical properties, such as tone, stiffness, or elasticity 6,7 . Many medical treatments and rehabilitative approaches are used to regulate the muscle tone, stiffness, or elasticity in stroke patients with upper limb impairment. A reliable and valid method for measuring muscle tone, stiffness and elasticity could show the effectiveness of these treatment modalities, the progression, and the success of interventions.
There are some options used to measure muscle mechanical properties. These methods have some advantages and disadvantages. The Modi ed Ashworth Scale is (MAS) the most widely used method to evaluate muscle tone. The MAS allows a practical and rapid assessment for measuring muscle tone; however, it is not su ciently sensitive to detect small changes in muscle tone, does not allow the measurement of activated muscle tone, and does not assess the tone of an isolated muscle 8,9 . Furthermore, the magnetic resonance and ultrasonography provide reliable and valid assessment of the soft tissue stiffness; however, these devices are expensive, take too much time, and do not allow the assessments to be performed in different environments. Because of these reasons, magnetic resonance imaging and ultrasonography are not too suitable to use in clinical practises. On the other hand, the myotonometer is a portable device which allows assessments to be performed in different environments.
In addition, it is a simple device, and one can learn how to use it easily.
There are various studies in the literature that investigated the reliability of the myotonometer. An important point of these studies was that they were conducted in healthy participants. There are a few studies which investigated the reliability of the myotonometer for measuring muscle mechanical properties in stroke patients. However, some of them were conducted in patients with acute stroke [10][11][12] , and some of them used the Myoton-3 myometer (a previous version of MyotonPRO) 10,13,14 . On the other hand, inter-rater reliability of the MyotonPRO was only investigated in patients with acute stroke by one study 11 . To our knowledge, there is no study which investigated the reliability of the MyotonPRO in patients with chronic stroke. Therefore, the purpose of the present study was to investigate the inter-rater and intra-rater reliability of the MyotonPRO for measuring the mechanical properties of the upper limp muscles in patients with chronic stroke. It was hypothesized that MyotonPRO would have su cient interrater and intra-rater reliability to measure the mechanical properties of the upper limp muscles in patients with chronic stroke.

Sample-Size Calculation
Simple size calculation was performed to determine the minimum sample size. Sample size calculation was performed based on an expected intraclass correlation coe cient of 0.85, a desired power level of 80%, and an alpha level of 0.5. The sample size calculation showed that the study must be conducted with at least 15 participants 15,16 .

Participants
The study was conducted in 20 stroke patients (14 males, 6 females) in an age range of 36-84 years (65.1 ± 11.2 years). Chronic stroke patients with a stroke onset of at least 6 months were included in the study. Patients were excluded if they reported: (1) having a severe cognitive impairment, (2) having an onset of rst ever stroke less than 6 months or more than 18 months, (3) having other neurologic, neuromuscular, or orthopaedic disease, (4) having excessive spasticity in the upper limps that might prevent the patient from taking the measurement position, (5) using an anti-spastic drug (e.g., botulinum toxin type A) during the study period, (6) having body mass index more than 30 kg/m, and (7) performing any strenuous exercises within the 24 h prior to measurements.
The present study was approved by the Non-Invasive Clinical Research Ethics Board of Mersin University (Protocol Number: 2020/517). Oral and written informed consents were obtained from each participant prior to experiment. The present study was conducted in accordance with the relevant guidelines and regulations of the local institute.

Procedure
The oscillation frequency, stiffness, and logarithmic decrement of the biceps brachii, triceps brachii, deltoid, and upper trapezius muscles were selected to determine the inter-rater and intra-rater reliability of the MyotonPRO. The measurements were conducted by two physiotherapists. Before the study, both evaluators practiced MyotonPRO on the muscles being evaluated to minimize the learning effect caused unfamiliarity with the device. Each participant was evaluated at 30-minute intervals by two evaluators. Both raters were unaware of the results during the measurements. A physiotherapist repeated the measurements 3 days after the rst measurements to assess the intra-rater reliability of the device. The measurements of the oscillation frequency, stiffness, and logarithmic decrement were performed at the same time of the day (± 1 h). For each muscle measured, 3 consecutive measurements were conducted at 30-second intervals and the average value of these 3 measurements was used for analysis.

Equipment
The oscillation frequency, stiffness, and logarithmic decrement of the biceps brachii, triceps brachii, deltoid, and upper trapezius muscles were measured using a MyotonPRO (Muomeetria Ltd., Tallinn, Estonia). The MyotonPRO measures mechanical oscillations in the evaluated tissue by applying a mechanical impulse with a short duration (15 milliseconds) and a constant mechanical force (up to 0.6 N). After applying mechanical impulse, measuring the mechanical oscillations provides the following data: (1) oscillation frequency (Hz), (2) stiffness (N/m), and (3) logarithmic decrement. Oscillation frequency (Hz) shows the tone of a muscle in its resting or passive state without any contraction.
Dynamic stiffness (N/m) provides information about its resistance to an external force or a contraction.
Logarithmic decrement provides about the information about the elasticity of the assessed soft tissue.
Elasticity shows the ability to return its previous shape after a removal of an external force or a contraction of deformation 17 .
The measurements of oscillation frequency, stiffness, and logarithmic decrement of the assessed muscles were performed on the effected side of the upper limb. Measurements were performed while the patient is sitting in a chair with a back support. Measurements were made while arm weight was in a position supported by a pillow, elbow at 45 ° exion, shoulder at 45° elevation, and the forearm was between pronation and supination. For the upper trapezius measurements, the probe of the device was positioned at 2 cm lateral of the midway between the lateral edge of the spinous process of C7 and acromion. The biceps brachii measurements were performed at the long head of the muscle in the middle of the arm. The triceps brachii measurements were performed at the medial head of the muscle in the middle of the arm. Deltoid measurements were performed at the middle part of the muscle in the plumpest portion of the muscle.

Statistical Analysis
Statistical analyses were conducted using a software program (SPSS version 22, IBM Corporation, Armonk, New York, USA). Descriptive data are presented as mean and standard deviation for the assessed parameters. Intraclass correlation coe cient (ICC) was used to determine the reliability of the device. The intra-rater reliability of the device was tested using ICC 3,1 (2-way mixed model consistency).
The ICC 2,2 (2-way random-effect model, absolute agreement) was used to determine the inter-rater reliability. For every comparison, the standard error of measurement (SEM), the coe cient of variation (CV), and the minimum detectable change

Results
The mean time since cerebrovascular disease onset ± standard deviation was 9.70±3.31 months. Nineteen patients with stroke had a right hemiplegia. All patients had upper limb spasticity. Table 1 shows the demographic and clinical characteristics of the patients.
The results of the inter-rater reliability assessment are presented in Table 2 The results of the intra-rater reliability assessment are given in Table 3 Bland and Altman plots for the frequency of the pooled data of the assessed muscles are presented in Figures 1 and 2. Bland and Altman plots for all the assessed muscles in frequency, stiffness, and decrement parameters show that there was no systematic bias between the two raters as well as between the two testing time points.

Discussion
To our knowledge, this is the rst study investigating the intra-rater and inter-rater reliability of the MyotonPRO device in measuring the mechanical properties of the upper limp muscles in patients with chronic stroke. The hypothesis of this study was that the MyotonPRO would have enough inter-rater and intra-rater reliability to measure the mechanical properties of the upper limb muscles in stroke patients. In line with the hypothesis, it was found that the MyotonPRO had a good to excellent inter-rater and intrarater reliability (ICC: 0.72-0.97) for measuring the tone, stiffness, and elasticity of the biceps brachii, triceps brachii, deltoid, and upper trapezius muscles. The ICC values obtained indicated that the MyotonPRO has su cient reliability to measure the tone, stiffness, and elasticity of muscles in chronic stroke patients 18,19 . In addition, CV values were below 11% in all assessed parameters. A CV value of less than 15% is allowed for measuring biological material. Furthermore, Bland-Altman analysis, which was used to identify potential systematic bias between measurements. The Bland-Altman analysis results showed that there was no systematic bias for all the muscles assessed, which showed consistency between the two measurements performed.
There are a few studies which investigated the inter-rater reliability of myotonometers in stroke patients.
Chuang et al. 14 investigated the intra-rater reliability of the Myoton-3 myometer, which is a previous version of the MyotonPRO. They reported that Myoton 3 has good to excellent reliability (ICC: 0.72-0.96) for measuring the tone, elasticity, and stiffness of the biceps brachii and triceps brachii muscles 14 .
Moreover, Chuang et al. 13 indicated that the Myoton-3 myometer had excellent intra-rater reliability (ICC: 0.83-0.95) for measuring the tone, stiffness, and elasticity of the deltoid, triceps brachii, biceps brachii, extensor digitorum, exor carpi radialis, and exor carpi ulnaris muscles in stroke patients. In a different study by Chuang et al. 10 , it was reported that the Myoton-3 myometer is a reliable device for measuring the tone, elasticity, and stiffness of the triceps brachii and bilateral biceps muscles in patients with subacute stroke, with a good to excellent intra-rater reliability (ICC: 0.72-0.96). Furthermore, Lo et al. 12 assessed the between-days reliability of the MyotonPRO for measuring the tone of the biceps brachii, brachioradialis, rectus femoris, and tibialis anterior muscles in acute stroke patients. They performed the measurement on two consecutive days to detect the between-days reliability of the MyotonPRO. They found that the MyotonPRO had a good to excellent reliability (ICC: 0.81-0.82) corresponding to SEM less than 1.24 Hz, and smallest real difference less than 3.08 Hz 12 . Lo et al. 11 investigated the inter-rater reliability of the MyotonPro for measuring the tone, stiffness, and elasticity of the biceps brachii, brachioradialis, rectus femoris, and tibialis anterior. They found a good to excellent inter-rater reliability in measuring the muscle mechanical properties (ICC: 0.63-0.97) 11 . There is a consensus in studies regarding the reliability of myotonometers. There seems to be a consensus in the literature that myotonometers are a reliable tool for measuring muscle mechanical properties; however, some of these studies investigated the intra-rater reliability of the Myoton-3 myometer 10,13,14 , and some of them included patients with acute stroke [10][11][12] . The results of the present study, which support the results of the studies in the literature, indicated that the MyotonPRO is a reliable tool also in patients with chronic stroke.
The present study has some limitations. Firstly, the present study was conducted in stroke patients with mild or moderate spasticity to be able to place them in a suitable measuring position. The results of the reliability assessment of the MyotonPRO would be different in patients with severe spasticity. Second, the measurements were performed in a rest state. The reliability of the device may be different in muscle contracted conditions or in a tension state. Lastly, the reliability of the MyotonPRO in stroke patients was investigated in super cial and larger skeletal muscles. Further studies regarding the reliability of the MyotonPRO in small muscle groups, muscle contracted conditions, or tension states in patients with chronic stroke are warranted.

Conclusion
The results obtained show that the MyotonPRO has a good to excellent intra-rater and inter-rater reliability for measuring the tone, stiffness, and elasticity of the deltoid, biceps brachii, triceps brachii, and upper trapezius muscles in patients with chronic stroke. The ndings demonstrated that the MyotonPRO is a reliable and repeatable tool for quantifying the muscle mechanical properties in stroke patients. The MyotonPRO can be used for the diagnostic and therapeutic intentions.
Practical implications.
Inter-observer reliability of MyotonPRO ranged from good to excellent.
Inter-day reliability of MyotonPRO ranged from good to excellent.
Coe cient of variation values were in a range from 3.9-11.0%.
MyotonPRO is a repeatable tool to quantify the muscle mechanical properties.

Declarations
Con ict of Interest Disclosure: None This research did not receive any speci c grant from funding agencies in the public, commercial, or notfor-pro t sectors.

Data Availability
All data included in this study are available upon request by contact with the corresponding author.