Quantitative measurement of resistance force and subsequent attenuation during passive isokinetic extension of the wrist in patients with mild to moderate spasticity after stroke

In the present study, we applied mechanical passive stretch with a custom-made motor-controlled device to the hemiparetic wrist in 17 participants with spasticity following stoke. The isokinetic passive extensive displacement of wrist flexor muscles with the device induced resistant reflex forces and subsequent depression of these forces. The indices obtained from maximum RF and the subsequent force reduction after maximum extension (damping force ratio and damping impulse ratio) increased in a velocity-dependent manner and showed significant velocity-dependent correlations with average MAS scores. When the MAS evaluation for the finger flexors was added to the MAS for the wrist flexors, the correlations became stronger. Furthermore, when the patients were divided into a mild group (average MAS 1or less) and a moderate group (average MAS more than 1), both the damping force ratio and the damping impulse ratio showed significantly higher values in the moderate group at angular velocities of 60 deg/s and 90 deg/s. Although MAS shows poor reliability at the lower end of the scale [14] and all of the patients in this study had average MAS scores of 3 (out of 0–5) or less in both fingers and wrist flexors, significant differences were detected between the mild and moderate groups at 60 deg/s and 90 deg/s. Measurements of the resistance to wrist extension with the current custom device may have detected changes similar to those felt in evaluating stiffness with MAS in a daily clinical setting, especially in patients with comparatively mild spasticity.

Previous studies measured joint stiffness including spasticity by considering a passive resistance force or torque in the wrist [34,35,36,37, 47], finger [38], elbow [30, 48], and ankle joints [25,26,27,28,29]. However, no studies have shown the correlation between the attenuated resistance force after the resistance peak and the MAS in hemiparetic patients with mild to moderate spasticity. This is the first report that focuses on the damping force after the peak resistance force induced by passive movement with isokinetic and motor-controlled velocity.

We often encounter a rapid rise of resistance in the latter half of the range of motion and subsequent weakening of resistance in patients with mild spasticity, when spastic muscle tone is measured manually in the clinic. In addition, the so-called clasp-knife phenomenon or the definition of the MAS (1 and 1 +), which refers to the attenuation of resistance after an increase in resistance, has been known for a long time and is considered to reflect the subsidence of electromyogram and resistance force [23, 40].

Although the force output by our device is probably different from that applied when spasticity is evaluated in the daily clinical setting, the measured changes in damping with isokinetic passive movements using the current device might reflect the mechanical changes that constitute the clasp-knife phenomenon and catch and release which we feel when evaluating a patient’s spasticity with MAS.

Normalization procedure

We calculated the ratio of the damping force to the maximum RF and that of the pure damping impulse to the total damping impulse, which may contribute to normalize the fluctuation of resistance due to the sliding mechanism, the effect of the setting position, and the difference in mechanical responsiveness to passive movement between individuals. Several studies have investigated the correlation between resistance to passive movement in various joints and the Ashworth Scale and MAS using a similar device [25,26,27,28,29, 34,35,36]. In addition, several studies have applied some ratio indices for normalized values [26, 27, 35], as we did in the current study. The correlation with MAS was clarified [27] and the difference between spastic and non-spastic patients in low-velocity passive movement was verified [26] only when the analysis was performed using normalized values.

In this study, normalization of the damping force and impulse through the use of a ratio might contribute to detect the difference at relatively low velocities, and to identify significant correlations with the average MAS.

On the other hand, there is an interesting study in which normalization was performed by subtracting the measured baseline torque at a very low speed which induced no spastic response based on the torque measured at a higher speed [38]. This method is considered to be a useful normalization that can remove the mechanical changes other than reflex torque that occur with passive extension. We expect that this normalization could cancel out the extra mechanical changes associated with the sliding mechanism in our device, and, in combination with the ratio normalization used in our study, it may result in a more rigorous extraction of the spasticity component.

In studies using mechanical resistance, it might sometimes be important to apply some normalization procedures when comparing resistance to clarify the differences between individual subjects.

Velocity-dependent resistance and correlation with the MAS

Spasticity has been defined as a velocity-dependent increase in resistance during passive stretch. Previous studies have reported that the maximum resistance against passive movements increased in a velocity-dependent manner [26, 27, 36, 49] and was correlated with the MAS [36]. However, in the current study, the maximum RF tended to decrease with velocity, while the normalized damping part tended to increase and showed significant correlations with the MAS in a velocity-dependent manner. One of the reasons why the resistance decreased in a speed-dependent manner in this study could be that measurements were performed in the order 30 deg/s, 60 deg/s, and 90 deg/s with a short interval. Previous studies have indicated that repetitive passive movements reduced reflex torque [50] in elbow flexors and post-activation depression in the soleus muscle [51]. In the wrist and finger flexors, the long latency component of the stretch reflex decreases at faster repetition rates [52]. As in the current study, it has been reported that resistance decreased in a velocity-dependent manner in patients with mild spasticity after stroke and was not correlated with MAS [40]. However, in the current study, we detected a velocity-dependent increasing tendency by focusing on the damping part, which has not been a focus of previous studies, and found significant correlations with MAS.

In previous studies, electromyographical and resistance changes in spastic muscles were investigated at various passive movement velocities from 5 to 500 deg/s in the wrist joint [34, 36, 37, 47, 53,54,55]. Among these studies, a few found a significant correlation between the velocity-dependent resistance component and MAS at low-velocity joint movements of 50–70 deg/s [36, 53], and our study also supports these findings. On the other hand, since the correlations and differences observed in the present study are more pronounced in a speed-dependent manner, further measurements at higher speeds may reveal larger damping changes and lead to more valid measurement results.

In the current study, the correlation between the damping part and the MAS became stronger when the MAS in finger flexors was added to the MAS in wrist flexors. Since the extrinsic finger muscles affect the passive component of wrist joint stiffness [55,56,57], it was considered that the stiffness of the extrinsic flexors of the fingers fixed to the device in the extended position may further affect the resistance to wrist extension. These changes in the correlations may indicate that the measured changes in force in the damping part quantitatively detect the spastic changes in wrist and finger flexors simultaneously. Typically, wrist spasticity is measured manually without all fingers extended. Since this device measures with the fingers extended, if spasticity of the extrinsic muscles of the fingers, such as the flexor digitorum superficialis (FDS) and flexor digitorum profundus (FDP), is strong, it is likely to reflect more spasticity in the finger flexors than in the wrist flexors, so care must be taken when interpreting measured values. If the equipment is modified to measure passive resistance force in both the extended and flexed finger positions, it may be possible to calculate spasticity of the extrinsic finger flexor muscles in addition to spasticity of the wrist flexors.

Kamper et al. [38] have shown in their finger spasticity measurement studies that the reduction in torque immediately after extrinsic finger flexors muscle extension caused by concurrent involuntary activity of the extensor digitorum communis (EDC). This finding has major implications for the “damping” that has been a focus of our research. Since the fingers are fixed to the hand plate in the extended position during measurement with our device, it is thought that the FDS and FDP are extended at the same time as passive extension of the wrist flexor muscles. Therefore, it is possible that the EDC muscle activity may have been evoked and influenced the damping force measured in this study. If EMG measurements of both flexor and extensor muscles can be performed simultaneously with our device, and if the aforementioned measurements during finger flexion and extension can be compared, this should provide a better understanding of the changes in damping forces associated with wrist flexor and finger flexor extension.

Force components that make up the damping force

The damping part that we focused on might be mainly associated with a neural component that includes spasticity. According to several studies, the resistance generated by passive wrist dorsiflexion consists of inertia, elasticity, viscosity, and neural components caused by muscle stretch reflexes [36, 48]. In post-stroke patients, Lindberg et al. [36] showed that there are individual differences in the magnitude of passive resistance and in the composition of each component. However, for these components, the viscosity and neural components change in a velocity-dependent manner, and the elastic component continues with constant resistance and increases at the end of the range of extension. Additionally, the proportion of neural components in the total resistance is relatively large [36]. On the other hand, inertia appears and disappears for a short time at the start of the increase in resistance and just before reaching the maximum range of extension [27, 36]. Based on these reports, the resistance damping part that we focused on in the current study could have arisen from both the viscosity and the neural components and the damping part might be mainly associated with the neural component including spasticity, since that part depended on velocity and appeared after the wrist joint reached the maximum range of extension.

Limitations

In several previous studies that measured torque and force for the assessment of joint stiffness or spasticity, the measurements of passive resistance were conducted only after sufficient time intervals. In the current study, continuous sessions with pauses of only several seconds were performed with a short rest of 1 to 2 min in the ascending order of velocity (30 deg/s, 60 deg/s, and 90 deg/s) in all subjects. The resistance forces were considered to be affected by attenuation due to repetition. Decrease of maximum RF by repetitive measurement at each velocity (Table 3) and the significant velocity-dependent decrease in total damping impulse (Fig. 3) may indicate that the overall resistance change decreased with repetition. The measurement intervals could have been longer [27, 36] and the angular velocities could have been measured randomly [26] or in a different order [36].

In the intra-rater reliability test, the reliability of the single measurement was partially poor, especially for the ratio index. To obtain more reliable data with less patient burden, it is necessary to examine measurement methods to obtain reliable results with fewer repetitions.

The ingenuity of the sliding mechanism could contribute to cancel out excessive tension on the wrist joint, while the resistance force fluctuated due to movement of the positional relationship of the hand with respect to the pressure-measurement part of the tension/compression load cell. Furthermore, when the hand and forearm were fixed to the device, misalignment of the wrist joint axis could occur, and therefore it would be necessary to address inter-rater reliability and the measurements in healthy controls.

Some studies have questioned the reliability and validity of the MAS used in this study [58, 59]. In an attempt to improve the reliability of MAS measurement data, measurements were taken by two therapists. However, inter-rater reliability for the two measurers in this study was also poor for both wrist and finger flexors.

Ansari et al. modified the MAS by deleting grade 1 + and redefining grades 1 and 2, to give the Modified Modified Ashworth Scale (MMAS), which has an ordinal relationship [58, 60, 61]. In the MMAS, the modified portion is defined as follows: 1 = slight increase in muscle tone, manifested by a catch and release or by minimal resistance at the end of the ROM when the affected part is moved in flexion or extension; 2 = marked increase in muscle tone, manifested by a catch in the middle range and resistance throughout the remainder of the ROM, but the affected part is easily moved. Given the reported good reliability [62, 63] and validity [64] of the MMAS for wrist flexors, we expect that this scale can be used to more accurately validate the measurements of this device.

In the analysis in this study, it is somewhat problematic that MAS, which is a nominal measure, was treated as an ordinal measure. Also, since the sample size was small, it would have been better to examine a larger number of subjects in stratified or categorized analyses.

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