**3. Metric properties of the myotonometric measurements: Reliability and validity**

Metric properties of the myotonometric measurements, such as reliability, validity, and responsiveness are the prerequisites of a useful measurement. From literature review, previous studies focused on examining reliability and validity of myotonometric measurement. The results of previous reliability studies have indicated that myotonometry is highly reliable for measuring skeletal muscle viscoelastic parameters in healthy individuals (Bizzini & Mannion, 2003; Ditroilo et al., 2011; Gavronski et al., 2007; Leonard et al., 2004; Leonard et al., 2003; Viir et al., 2006), children with cerebral palsy (Aarrestad et al., 2004; Lidstrom et al., 2009), and patients with Parkinson's disease (Marusiak et al., 2010; Ratsep & Asser, 2011). There is no study investigating the reliability of the myotonometer in stroke patients, which may limit the interpretation of the change for myotonometric measurements.

The construct validity of the myotonometer has been established in healthy individuals (Gubler-Hanna et al., 2007), patients with upper motor neuronal disorders (Leonard et al., 2001), and stroke survivors (Rydahl & Brouwer, 2004). Studies have shown that muscle stiffness increased with increasing contractile force and muscle activation, indicating that muscle stiffness during contracted conditions provides an indirect measure of muscle strength (Aarrestad et al., 2004; Bizzini & Mannion, 2003; Gubler-Hanna et al., 2007; Leonard et al., 2001; Rydahl & Brouwer, 2004). Moreover, Katz and Rymer (1989) demonstrated that extending a limb against passive resistance may be more related to the viscoelastic properties of the soft tissues than to spasticity, indicating that biomechanical measures correlate most closely with motor function. These findings provide the theoretic basis for use of muscle strength and motor function measures to further validate myotonometric measures.

## **4. Metric properties of the myotonometric measurements: Reliability, validity, and responsiveness of the Myoton-3 myometer in patients with stroke**

Previous metric studies of myotonometry have not yet reported the responsiveness. The responsiveness of the instrument is its ability to detect change over time, which is an important quality to detect small changes in muscle properties and assess the effectiveness of specific treatment. Additionally, previous reliability and validity studies applied the myotonometer on large muscles of the trunk and extremities. Wrist and finger control is the motor function most likely to be impaired after stroke. Proper function of the muscles involved in hand movements is crucial to manual exploration and manipulation of the environment.

Our recent study (Chuang et al., 2012) addressed the test-retest reliability, validity, and responsiveness of the Myoton-3 myometer used for assessing tone, elasticity, and stiffness of the affected forearm muscles under a relaxed state in stroke rehabilitation. The Myoton-3 myometer represents a new technology to quantify mechanical properties of resting and contractiling muscles. To the best of our knowledge, this was the first report to show the metric soundness of the Myoton-3 myometer for assessing muscle tone, elasticity, and stiffness of the extensor digitorum, flexor carpi radialis, and flexor carpi ulnaris muscles in patients with stroke. Information reported in this study that is relevant to purposes of this book chapter is summarized below.

#### **4.1 Study sample**

40 Rehabilitation Medicine

From discerning muscular properties using myotonometric measurements, clinicians would be able to have a better understanding of the pathologic processes of muscle functions in individuals with spastic muscle secondary to stroke, design a specific rehabilitation program for each patient, make appropriate clinical decision, plan a more targeted and customized treatment specifically for each patient with abnormal muscle properties, and assess the efficacy of specific therapeutic treatment (Pandyan et al., 1999; Wade, 1992). This chapter will illustrate the metric properties of myotonometric measurement based on previous

**3. Metric properties of the myotonometric measurements: Reliability and** 

Metric properties of the myotonometric measurements, such as reliability, validity, and responsiveness are the prerequisites of a useful measurement. From literature review, previous studies focused on examining reliability and validity of myotonometric measurement. The results of previous reliability studies have indicated that myotonometry is highly reliable for measuring skeletal muscle viscoelastic parameters in healthy individuals (Bizzini & Mannion, 2003; Ditroilo et al., 2011; Gavronski et al., 2007; Leonard et al., 2004; Leonard et al., 2003; Viir et al., 2006), children with cerebral palsy (Aarrestad et al., 2004; Lidstrom et al., 2009), and patients with Parkinson's disease (Marusiak et al., 2010; Ratsep & Asser, 2011). There is no study investigating the reliability of the myotonometer in stroke patients, which may limit the interpretation of the change for myotonometric

The construct validity of the myotonometer has been established in healthy individuals (Gubler-Hanna et al., 2007), patients with upper motor neuronal disorders (Leonard et al., 2001), and stroke survivors (Rydahl & Brouwer, 2004). Studies have shown that muscle stiffness increased with increasing contractile force and muscle activation, indicating that muscle stiffness during contracted conditions provides an indirect measure of muscle strength (Aarrestad et al., 2004; Bizzini & Mannion, 2003; Gubler-Hanna et al., 2007; Leonard et al., 2001; Rydahl & Brouwer, 2004). Moreover, Katz and Rymer (1989) demonstrated that extending a limb against passive resistance may be more related to the viscoelastic properties of the soft tissues than to spasticity, indicating that biomechanical measures correlate most closely with motor function. These findings provide the theoretic basis for use of muscle strength and

**4. Metric properties of the myotonometric measurements: Reliability, validity,** 

Previous metric studies of myotonometry have not yet reported the responsiveness. The responsiveness of the instrument is its ability to detect change over time, which is an important quality to detect small changes in muscle properties and assess the effectiveness of specific treatment. Additionally, previous reliability and validity studies applied the myotonometer on large muscles of the trunk and extremities. Wrist and finger control is the motor function most likely to be impaired after stroke. Proper function of the muscles involved in hand movements is crucial to manual exploration and manipulation of the

**and responsiveness of the Myoton-3 myometer in patients with stroke** 

motor function measures to further validate myotonometric measures.

studies and our recent research in stroke rehabilitation.

**validity** 

measurements.

environment.

We recruited 67 patients (40 men and 27 women) who were a mean age of 54.67 (SD, 10.90) years. The mean time since the stroke onset was 21.12 (SD, 13.63) months, and 31 patients had left hemiplegia. All participants had sustained a first-ever stroke, Brunnstrom stage III to V for the proximal and distal upper extremity (UE) (Brunnstrom, 1970), MAS ≤ 2 in any joint of the UE (Bohannon & Smith, 1987), no cognitive impairment (Mini-Mental State Examination score ≥ 24) (Folstein et al., 1975), not participated in any experimental rehabilitation or drug studies, and not used anti-spasticity drugs for the UE musculature (e.g., botulinum toxin type A) during the study period. Institutional Review Board approval was obtained from the study sites, and written informed consent was obtained from each patient before inclusion.

#### **4.2 Instrument**

The functional state of the participants' skeletal muscles was assessed by using myotonometric measurements with the Myoton-3 myometer, created at the University of Tartu in Estonia (Vain, 1995).

The Myoton-3 myometer has a two-armed lever. On the long lever is the testing end and on the short lever is the core of the electromagnet. The essence of the method lies in giving the muscle a short mechanical impulse to evoke decaying oscillations of the muscle because of the elastic behavior of the muscle. The working principles of the Myoton-3 myometer were as follows: the testing end of the Myoton-3 was placed perpendicular to the skin surface above the muscle to be measured and a brief mechanical impulse was applied, shortly followed by a quick release to the muscle through an acceleration probe. The characteristics of the muscle deformation and also the damped oscillations of the muscle evoked after the quick release of the testing end were recorded by the acceleration transducer at the testing end of the device. At the moment the Myoton-3 myometer pickup has created the maximum compression of the tested muscle, the corresponding acceleration amax characterizes the resistance force of the muscle for the deformation depth Δ*l* (Figure 1).

The parameters of the graph characterize the functional state of the muscle. Displacement (s) is the difference in the initial position of the tested muscle and its final position. The relationships between position, velocity, and acceleration form an important application of the definite derivative. The velocity is defined by the derivative of position at a given time; whereas the acceleration is defined by the derivative of velocity at a given time. The average velocity of the muscle is the total displacement during an extended period of time, divided by that period of time. Average acceleration is the total change in velocity over an extended

Myotonometric Measurement of Muscular Properties of Hemiparetic Arms in Stroke Patients 43

The logarithmic decrement of the damping oscillations characterizes muscle elasticity, which is the ability of the muscle to restore its initial shape after contraction. Elasticity is inversely proportional to the decrement. If the decrement of trained muscles decreases, the muscle elasticity increases. The decrement values are usually 1.0 to 1.2, depending on the

Decrement = ln (amax / a) where amax is the maximal amplitude of oscillation and a is the oscillation amplitude (Figure 1). Stiffness (N/m) reflects the resistance of the muscle to the force deforming the muscle (Roja et al., 2006). The usual range of stiffness values is 150 to 300 N/m for resting muscle and may exceed 1000 N/m for contracted muscles (Gapeyeva & Vain, 2008). Stiffness was

Stiffness (N/m) = *f* / Δ*l* = *m* × amax / Δ *l* where *f* is the force applied, *m* is the mass of the testing end (kg), amax is the maximal acceleration of oscillation (meter/second2), and Δ *l* is the deformation depth of the muscle

Myotonometric testing of the affected extensor digitorum, the flexor carpi radialis, and the flexor carpi ulnaris in relaxed state was conducted before and after treatments. All participants received a 1.5-hour therapy session 5 times per week for 4 weeks. A senior occupational therapist administered the outcome measures at baseline and after the 4-week treatment. Before measurement, participants were informed about standard measurement procedure with their elbow flexion 30° to 45°, the palm downward for the affected extensor digitorum measurement and palm upward for measurements of the affected flexor carpi radialis and ulnaris muscles (Figure 2) (Gapeyeva & Vain, 2008). The investigator applied resistance to the tested muscles and requested participants to make an effort to resist. At the same time, the investigator established the location of the tested muscles by the visualpalpatory test. Participants were instructed to lie supine and relax the muscles maximally. Three trials were recorded with a 1-second interval, and the average value was used for analysis. To investigate test-retest reliability, 58 of the 67 individuals were tested twice on

(A) (B) (C)

Fig. 2. The standard measurement location of the measured muscles: (A) extensor

digitorum, (B) flexor carpi radialis, and (C) flexor carpi ulnaris

muscle. The logarithmic decrement of damping was calculated as:

(meter) (Figure 1).

**4.3 Procedures** 

calculated as a ratio between the force applied and the muscle deformation:

the affected side with the same procedure, 30 minutes apart, at baseline.

period of time, divided by the duration of that period. In Figure 1, time moment 1 (t1) denotes the beginning of the mechanical impulse to the muscle. The maximum of the deformation speed is obtained at time moment 3 (t3) and from that moment the muscle deformation speed decreases and at time moment 4 (t4) the acceleration transducer of the device has reached the maximum depth of its trajectory inward the muscle. At time moment 5 (t5) the forces of muscle elasticity have given to the transducer its maximum speed upwards. At time moment 6 (t6) this speed has decreased to zero under the influence of gravity. The above-described process repeats itself until the oscillation has decayed completely.

Fig. 1. An oscillation graph of the muscle shows the acceleration (a), velocity (v), and displacement (s) of the muscle produced in the process of damped natural oscillation measured by the Myoton-3 myometer.

The parameters measured by the myotonometer are oscillation frequency, decrement, and stiffness. The acceleration value of the first period of oscillations characterizes the deformation of the muscle, and the value of the next oscillation period provides the basis for calculating the oscillation frequency (Hz). The oscillation frequency is usually 11 to 16 Hz in relaxation and 18 to 40 Hz in contraction, depending on the muscle (Gapeyeva & Vain, 2008). The frequency of the damped oscillations characterizes the muscle tone, the mechanical tension in a relaxed muscle. The higher the value, the more tense is the muscle. The frequency of the damping was calculated as:

Frequency (Hz) = 1 / T

where T is the oscillation period in seconds (Figure 1).

The logarithmic decrement of the damping oscillations characterizes muscle elasticity, which is the ability of the muscle to restore its initial shape after contraction. Elasticity is inversely proportional to the decrement. If the decrement of trained muscles decreases, the muscle elasticity increases. The decrement values are usually 1.0 to 1.2, depending on the muscle. The logarithmic decrement of damping was calculated as:

#### Decrement = ln (amax / a)

where amax is the maximal amplitude of oscillation and a is the oscillation amplitude (Figure 1).

Stiffness (N/m) reflects the resistance of the muscle to the force deforming the muscle (Roja et al., 2006). The usual range of stiffness values is 150 to 300 N/m for resting muscle and may exceed 1000 N/m for contracted muscles (Gapeyeva & Vain, 2008). Stiffness was calculated as a ratio between the force applied and the muscle deformation:

$$\text{Stiffness (N/m)} = f / \,\Delta l = m \times \mathbf{a}\_{\text{max}} \, / \,\, \Delta l$$

where *f* is the force applied, *m* is the mass of the testing end (kg), amax is the maximal acceleration of oscillation (meter/second2), and Δ *l* is the deformation depth of the muscle (meter) (Figure 1).

#### **4.3 Procedures**

42 Rehabilitation Medicine

period of time, divided by the duration of that period. In Figure 1, time moment 1 (t1) denotes the beginning of the mechanical impulse to the muscle. The maximum of the deformation speed is obtained at time moment 3 (t3) and from that moment the muscle deformation speed decreases and at time moment 4 (t4) the acceleration transducer of the device has reached the maximum depth of its trajectory inward the muscle. At time moment 5 (t5) the forces of muscle elasticity have given to the transducer its maximum speed upwards. At time moment 6 (t6) this speed has decreased to zero under the influence of gravity. The above-described process

Fig. 1. An oscillation graph of the muscle shows the acceleration (a), velocity (v), and displacement (s) of the muscle produced in the process of damped natural oscillation

The parameters measured by the myotonometer are oscillation frequency, decrement, and stiffness. The acceleration value of the first period of oscillations characterizes the deformation of the muscle, and the value of the next oscillation period provides the basis for calculating the oscillation frequency (Hz). The oscillation frequency is usually 11 to 16 Hz in relaxation and 18 to 40 Hz in contraction, depending on the muscle (Gapeyeva & Vain, 2008). The frequency of the damped oscillations characterizes the muscle tone, the mechanical tension in a relaxed muscle. The higher the value, the more tense is the muscle.

Frequency (Hz) = 1 / T

measured by the Myoton-3 myometer.

The frequency of the damping was calculated as:

where T is the oscillation period in seconds (Figure 1).

repeats itself until the oscillation has decayed completely.

Myotonometric testing of the affected extensor digitorum, the flexor carpi radialis, and the flexor carpi ulnaris in relaxed state was conducted before and after treatments. All participants received a 1.5-hour therapy session 5 times per week for 4 weeks. A senior occupational therapist administered the outcome measures at baseline and after the 4-week treatment. Before measurement, participants were informed about standard measurement procedure with their elbow flexion 30° to 45°, the palm downward for the affected extensor digitorum measurement and palm upward for measurements of the affected flexor carpi radialis and ulnaris muscles (Figure 2) (Gapeyeva & Vain, 2008). The investigator applied resistance to the tested muscles and requested participants to make an effort to resist. At the same time, the investigator established the location of the tested muscles by the visualpalpatory test. Participants were instructed to lie supine and relax the muscles maximally. Three trials were recorded with a 1-second interval, and the average value was used for analysis. To investigate test-retest reliability, 58 of the 67 individuals were tested twice on the affected side with the same procedure, 30 minutes apart, at baseline.

Fig. 2. The standard measurement location of the measured muscles: (A) extensor digitorum, (B) flexor carpi radialis, and (C) flexor carpi ulnaris

Myotonometric Measurement of Muscular Properties of Hemiparetic Arms in Stroke Patients 45

Results of the ANOVA showed a significant difference in muscle tone, elasticity, and stiffness among the 3 affected muscles before and after treatment (*P* < 0.0001). Post hoc analyses revealed that muscle tone and stiffness of the extensor digitorum were significantly higher than those of the flexor carpi radialis and flexor carpi ulnaris at both pretreatment and posttreatment (pretreatment tone and stiffness: *P* < 0.0001, posttreatment tone: *P* < 0.0001, posttreatment stiffness: *P* = 0.008, *P* < 0.0001, resepctively). Muscle tone of the flexor carpi radialis was significantly higher than that of flexor carpi ulnaris at pretreatment and posttreatment (*P* = 0.025, 0.002, respectively). Muscle stiffness of the flexor carpi radialis was significantly higher than that of flexor carpi ulnaris at posttreatment (*P* = 0.001). Muscle elasticity of the extensor digitorum was significantly lower than the elasticity of flexor carpi radialis and flexor carpi ulnaris at both pretreatment and posttreatment (*P*< 0.0001, *P*< 0.0001, respectively). In general, the extensor digitorum showed higher tone and stiffness

The test-retest reliability was performed on a subset of 58 participants who underwent two pretreatment measurements. The Myoton-3 myometer showed high to very high test-retest reliability for muscle properties in affected extensor digitorum, flexor carpi radialis, and

Our study indicated that the Myoton-3 is a highly reliable measurement tool with high testretest reliability under relaxed conditions in measurements of affected forearm muscles of stroke patients. These findings are similar to those reported of the myotonometer for different muscles and study populations. The reliability of the myotonometer was high in the biceps brachii, rectus femoris, biceps femoris, and gastrocnemius in healthy individuals (Bizzini & Mannion, 2003; Ditroilo et al., 2011; Leonard et al., 2003; Marusiak et al., 2010); the biceps brachii in patients with Parkinson's disease (Marusiak et al., 2010); and in the brachii, gastrocnemius, and rectus femoris in children with cerebral palsy (Aarrestad et al., 2004; Lidstrom et al., 2009). In general, the Myoton-3 myometer is reliable for measurements in

Significant correlations existed between the tone and stiffness of the 3 muscles and palmar pinch strength, between those of the flexor carpi radialis & ulnaris muscles and lateral pinch strength, and between those of the flexor carpi radialis and the ARAT at posttreatment. The posttreatment elasticity of the two flexor carpi muscles was significantly correlated with grip strength. The pretreatment elasticity of the flexor carpi ulnaris was significantly correlated with posttreatment grip strength, and the pretreatment muscle tone and stiffness of the flexor carpi radialis were significantly correlated with palmar pinch strength and ARAT. There was no significant correlations existed between the Brunnstrom stage and muscle properties of the 3 muscles at pretreatment. Posttreatment extensor digitorum tone and flexor carpi radialis stiffness

The results of the concurrent validity showed partly significant associations between forearm muscle properties and hand strength and UE motor function, especially at

with lower elasticity compared to the flexor carpi radialis and ulnaris muscles.

**4.6.2 Reliability of the Myoton-3 myometer in patients with stroke**

healthy individuals as well as for various patient populations.

were significantly correlated with the Brunnstrom stage.

**4.6.3 Validity of the Myoton-3 myometer in patients with stroke** 

flexor carpi ulnaris (ICC, 0.86-0.96).

## **4.4 Criterion measures**

The Myoton-3 measures, as well as criterion measures for hand strength, including grip strength, lateral pinch power, and palmar pinch power, the Action Research Arm Test (ARAT), and Brunnstrom stage were performed before and after treatments.
