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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 65  |  Issue : 3  |  Page : 109-116

Evaluation of post-stroke spasticity from the subacute to chronic stages: A clinical and neurophysiologic study of motoneuron pool excitability


1 Department of Physical Medicine and Rehabilitation, Cheng Hsin General Hospital, Taipei, Taiwan
2 Department of Physical Medicine and Rehabilitation, Cheng Hsin General Hospital, Taipei; Graduate Institute of Gerontology and Health Care Management, Chang Gung University of Science and Technology, Taoyuan, Taiwan
3 Department of Neurosurgery, Cheng Hsin General Hospital, Taipei, Taiwan
4 Department of Medical Education, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan
5 Department of Physical Medicine and Rehabilitation, Cheng Hsin General Hospital; Department of Physiology and Biophysics, National Defense Medical Center, Taipei, Taiwan

Date of Submission25-Feb-2022
Date of Decision11-Apr-2022
Date of Acceptance16-Apr-2022
Date of Web Publication27-Jun-2022

Correspondence Address:
Dr. Szu-Fu Chen
No. 45, Zhenxing St., Beitou, Taipei 112401
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0304-4920.348359

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  Abstract 


Spasticity measured using clinical scales, such as the modified Ashworth scale (MAS), may not sufficiently evaluate the effectiveness of therapeutic interventions and predict prognosis. This study aimed to compare changes in H-reflex excitability in the spastic and unimpaired upper and lower limbs of patients with acute and chronic stroke. We also investigated the relationship between the degree of spasticity as assessed by the MAS and motor neuron pool excitability with by analyzing H-reflex excitability. Sixty adult patients with a first-ever stroke were recruited for this study. MAS scores were recorded in the post-stroke upper and lower limb muscles. H-reflexes and M-responses of the bilateral flexor carpi radialis and soleus were tested by stimulating the median and tibial nerves. The results showed that both the ratio of the maximal size of the H-reflex (Hmax) to the maximal size of the M-response (Mmax) and the ratio of the developmental slope of H-reflex (Hslp) to that of the M-responses (Mslp) were significantly higher on the spastic side than on the unimpaired side for the upper and lower limbs. In contrast, the ratio of the threshold of the H-reflex (Hth) to the threshold of the M-response (Mth) only showed significant differences between the two sides in the upper limbs. The Hslp/Mslp paretic/non-paretic ratio was increased in patients with MAS scores of 2 or 3 compared to MAS scores of 1 for both the upper and lower limbs, whereas the Hmax/Mmax paretic/non-paretic ratio showed significant differences between MAS scores of 2 or 3 and 1 only in the upper limbs. Moreover, in either the spastic or unimpaired sides, there were no significant differences in any of the three motoneuron pool excitability parameters, Hmax/Mmax, Hslp/Mslp, and Hth/Mth, between the shorter chronicity (time post-stroke ≤6 months) and longer chronicity groups (time post-stroke >6 months) for both the upper and lower limbs. These results suggest that Hslp/Mslp could be a potential neurophysiological indicator for evaluating the degree of spasticity in both the upper and lower limbs of patients with hemiplegia. The MAS and Hslp/Mslp characterize clinical and neurophysiologic spasticity, respectively, and could be used as an integrated approach to evaluate and follow up post-stroke spasticity.

Keywords: H-reflex, modified Ashworth scale, M-wave, spasticity, stroke


How to cite this article:
Shen HY, Lin JY, Chen CC, Lee HF, Chao H, Lieu FK, Chen SF. Evaluation of post-stroke spasticity from the subacute to chronic stages: A clinical and neurophysiologic study of motoneuron pool excitability. Chin J Physiol 2022;65:109-16

How to cite this URL:
Shen HY, Lin JY, Chen CC, Lee HF, Chao H, Lieu FK, Chen SF. Evaluation of post-stroke spasticity from the subacute to chronic stages: A clinical and neurophysiologic study of motoneuron pool excitability. Chin J Physiol [serial online] 2022 [cited 2022 Aug 17];65:109-16. Available from: https://www.cjphysiology.org/text.asp?2022/65/3/109/348359




  Introduction Top


Stroke is the leading cause of serious long-term disability worldwide.[1] Spasticity is one of the most common complications in stroke survivors, occurring in approximately 40% of patients.[2] Throughout the evolution of stroke from the acute to the chronic stages, spasticity interacts with weakness, leading to impaired execution of normal motor behaviors. Spasticity and its related abnormal joint postures cause pain and diminished joint mobility, resulting in impaired motor control and functional limitations such as inability to grasp, reach, transfer, and walk.[3] This in turn, significantly affects patients' mobility and activities of daily living and limits their vocational and social participation. Clearly, objective clinical tools are needed to evaluate therapeutic interventions and predict the prognosis of spasticity.

The evaluation of spasticity has been mostly performed through a clinical approach based on neurological examination and the use of specific clinical scales.[4] The modified Ashworth scale (MAS) is the most commonly used clinical tool for measuring spasticity.[4] Although there are a few studies showing good inter-rater and intra-rater reliability of the MAS in evaluating post-stroke spasticity,[5],[6] it is still limited by the variability among different muscles and has low sensitivity to slight variations.[7],[8] In addition, the MAS only measures resistance to passive movement, which is only one aspect of spasticity and not a comprehensive assessment; thus, MAS scores may be influenced by several factors, including joint contractures, the expertise of evaluators, repeated testing, and temperature.[8] Accordingly, it is crucial to develop objective and quantitative assessments to determine the effects of preventative, pharmacological, and rehabilitative strategies on post-stroke spasticity.

The H-reflex is the reflectory reaction from afferent Ia sensory fibers through the motoneuron pool to efferent motor fibers; the M-response is the action potential from the stimulation of peripheral nerves through direct motor efferent fibers to the innervating muscle.[9] Several studies have shown that electrophysiological parameters using the H-reflex and M-response can measure spasticity more objectively and can be used as a part of clinical evaluation.[10],[11],[12],[13] The H-reflex, an electrically elicited spinal stretch reflex, is a conventional indicator used to evaluate spinal alpha motor neuron excitability in both clinical and research settings.[14] However, as the amplitude of the H-reflex varies among subjects, it is essential to normalize this value so that comparisons can be made between individuals. Recent studies have shown that other parameters, including the ratio of the maximal size of the H-reflex (Hmax) to the maximal size of the M-response (Mmax), the ratio of the threshold of the H-reflex (Hth) to the threshold of the M-response (Mth), or the ratio of the developmental slope of the H-reflex (Hslp) to that of the M-responses (Mslp) can measure spasticity more objectively.[10],[11],[12],[13],[15] In healthy adults, the value of Hmax/Mmax is usually below 0.75,[16] but the reference range of Hslp/Mslp and Hth/Mth have not been widely established yet. Due to higher motoneuron pool excitability in the stroke patients, the values of Hslp/Mslp and Hmax/Mmax are significantly higher in the spastic side than in the unimpaired side. However, the value of Hth/Mth is lower in the spastic side than in the unimpaired side as motor neurons of stroke patients exhibit higher excitability than that of normal people.[10],[15] Among them, Hslp/Mslp is proposed as the most valid and sensitive method because it is not affected by suppression of the H-reflex that is associated with the collision phenomenon.[15] However, previous studies have shown controversial results regarding the relationship between these three parameters and clinical scales. The soleus Hslp/Mslp of the spastic side was significantly higher than that of the unimpaired side in hemiplegic patients, but there was no correlation between MAS scores and Hslp/Mslp in patients with wrist flexor or ankle flexor spasticity after stroke.[10],[11],[17] Another study showed a significant positive correlation between MAS scores and both the Hslp/Mslp ratio and the traditional Hmax/Mmax index in stroke patients with wrist flexor spasticity.[12] Previous neurophysiological studies on post-stroke spasticity have mainly focused on patients with chronic stroke.[10],[11],[12],[13],[17] However, because spasticity starts to occur as abnormal neuroplasticity develops, and because the median time to detect spasticity is 1 month after stroke onset,[18] early identification of spasticity is crucial for adequate treatment and possibly better outcomes. Accordingly, the objectives of this study were as follows: (1) To compare changes in H-reflex excitability in spastic and unimpaired upper and lower limbs of both acute and chronic stroke patients and (2) to examine the relationship between the degrees of spasticity as assessed by the MAS and motor neuron pool excitability by three parameters, Hmax/Mmax, Hslp/Mslp, and Hth/Mth.


  Materials and Methods Top


Participants

Sixty adult patients with first-ever stroke diagnosed using computed tomography or magnetic resonance imaging that resulted in hemiplegia were recruited from a teaching hospital in Taiwan. The exclusion criteria were as follows: (1) Fixed muscle contractures in the affected arm or lower limb (muscle tone graded as 4/4 on the MAS); (2) bony deformities of the affected limbs; (3) other neurological or orthopedic conditions involving the affected limbs; and (4) inability to complete the experimental procedures for any reason. The study was conducted in accordance with the Declaration of Helsinki. Approval was granted by the Institutional Review Board of Cheng Hsin General Hospital (CHGH-IRB (868)110-14) in Taipei, Taiwan. All participants provided written informed consent prior to their participation in the study.

Procedure

The spasticity of the wrist flexors and ankle dorsiflexors was graded according to their MAS scores. These measurements were followed by H-reflex measurements. All clinical and neurophysiological measurements were performed by the same trained physiatrist in order to eliminate inter-rater variability. Demographic data pertaining to the patients were also recorded.

The modified Ashworth scale

Spasticity of the wrist flexors and ankle dorsiflexors was assessed clinically using a 5-point MAS, with the scores graded as follows: 0 = no increase in muscle tone; 1 = slight increase in muscle tone manifested by a catch and release or by minimal resistance at the end of the range of motion; 1+ = slight increase in muscle tone manifested by a catch, followed by minimal resistance throughout the remainder (less than half) of the range of motion; 2 = marked increase in muscle tone through most of the range of motion, but the affected part(s) are easily moved; 3 = considerable increase in muscle tone, passive movement difficult; and 4 = the affected part(s) are rigid.[6],[19] Resistance to passive muscle stretch was assessed at the wrist and ankle joints of the hemiplegic limb with the patient lying flat in the supine position.

Measurement of H-reflexes and M-responses

While the subject was lying supine for median nerve stimulation and prone for tibial nerve stimulation, electrophysiological tests were conducted at a mean room temperature of 25°C and skin temperature of 32°C–34°C. The H and M-waves were acquired using a Neuromapper EMG machine (Medelec Synergy Oxford Instruments Medical Systems, Surrey, UK), as similarly described by Christie et al.[20] The settings were as follows: bandpass filter, 5 Hz to 3 kHz; sweep rate, at 5 ms/div; and sensitivity, 500 μV to 2 mV/div (depending on the signal size). Rectangular electric pulses with a duration of 1 ms were repeated every 5 s to prevent habituation of the reflex response, with an output ranging from 0 to 100 mA. A bipolar stimulus probe was used to stimulate the median nerve at the elbow crease and the tibial nerve at the popliteal fossa. The self-adhesive surface-active electrodes were placed on the bellies of the flexor carpi radialis (FCR), with the reference electrode on the radial styloid process or the soleus muscle and with the reference electrode over the insertion of the Achilles tendon. A ground electrode was attached to the skin between the active electrode and the stimulus probe. Median nerve stimulation was performed with the forearm fully supinated. Tibial nerve stimulation was performed with the patient lying in the prone position with their feet suspended over the end of the bed and with their head on a pillow.

The stimulus intensity was gradually increased until an H-reflex without an M-response was recorded. The response with the largest amplitude was selected as the Hmax. The stimulus intensity was then increased in small increments until the maximum M-response was obtained. The maximal amplitude of the H-reflex and M-response (Hmax and Mmax, respectively) was defined as the point at which the amplitude did not increase with increasing stimulation intensity. At least five Hmax and Mmax values were analyzed to ensure reproducibility. The maximum amplitudes of the H-reflexes and M-wave amplitudes were measured from the peak of the positive to the peak of the negative deflections, and Hmax/Mmax was calculated by dividing the maximum amplitudes of the H-reflex by that of the M-wave. The H-reflex and M-response thresholds (Hth and Mth, respectively) were defined as the minimal stimulation intensity to evoke a detectable response, and Hth/Mth was calculated by dividing the minimal stimulation intensity of the H-reflex by that of the M-wave. To obtain both H-reflex and M-wave recruitment curves, the raw sizes of both the H-reflex and M-response were converted to relative sizes (ordinate) by dividing them by the mean maximal size of the M-response, which was calculated based on the 5 M-responses evoked at the highest intensity of electric stimulation. The slopes of the ascending (Hslp) and descending phases of the H-reflex recruitment curve and the ascending slope of the M-wave recruitment curve (Mslp) were derived from a linear regression line that included values from the transformed curve between 10% and 90% of the Hmax and Mmax values, respectively. Hslp/Mslp was calculated by dividing the slope of the H-reflex by that of the M-wave.[15]

Statistical analyses

Data are presented as the mean and standard deviation (mean ± SD). The Kruskal–Wallis test followed by post hoc Dunn's test was used for multiple groups to determine significant differences. The Student's t-test was used to test for differences between the two groups. Statistical significance was set at P < 0.05.


  Results Top


Demographic data

The study group comprised of 60 post-stroke patients (32 men, 28 women; mean age, 56.65 ± 11.68 years; range, 35–78 years). Forty-five percent of the patients had ischemic stroke. Stroke lesions were mostly located in the basal ganglion (53.3%) and middle cerebral artery (20%). Patients were classified into two groups according to the time post-stroke (mean ± SD): shorter chronicity (n = 26; ≤6 months; 3.3 ± 1.2 months) post-stroke and longer chronicity (n = 34; >6 months; 56.4 ± 39.9 months) post-stroke. The mean ages (range) of the patients in these two groups were 55.5 ± 11.1 (41–78) years and 57.5 ± 12.2 (35–74) years, respectively. The details of the patients' demographic and clinical data are presented in [Table 1]. There were no significant differences between the shorter and longer chronicity groups. Twenty-nine patients had impairment of the right side. All 60 patients completed H-reflex and M-wave examinations. In 2 of the 60 patients, the lower limb H-reflex could be evoked only on the spastic side. Thus, the mean and SD values of Hmax and Mmax, Hth and Mth, and Hslp and Mslp in the lower limbs were calculated only for the 58 patients in whom the lower limb H-reflex could be evoked on both sides.
Table 1: Demographic characteristics of the participants

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H-reflexes and M responses following stroke

We first compared motoneuron pool excitability parameters between the shorter and longer chronicity groups. On both the paretic and non-paretic sides, there were no significant differences among any of the three motor neuron pool excitability parameters, Hmax/Mmax, Hslp/Mslp, and Hth/Mth, between the two study groups in both the upper and lower limbs. The mean ± SD of the Hmax/Mmax, Hslp/Mslp, and Hth/Mth ratios in the paretic arms were 0.29 ± 0.18, 0.72 ± 0.59, and 0.92 ± 0.11 in the shorter chronicity group and 0.31 ± 0.20, 0.54 ± 0.42, and 0.90 ± 0.11 in the longer chronicity group, respectively [Table 2]. The Hmax/Mmax, Hslp/Mslp, and Hth/Mth ratios in the paretic legs were 0.5 ± 0.4, 0.94 ± 0.87, and 0.86 ± 0.16 in the shorter chronicity group and were 0.57 ± 0.42, 1.36 ± 1.14, and 0.81 ± 0.11 in the longer chronicity group, respectively [Table 2]. In the non-paretic arms, the mean ± SD Hmax/Mmax, Hslp/Mslp, and Hth/Mth ratios in the paretic arms were 0.10 ± 0.07, 0.21 ± 0.18, and 1.02 ± 0.1 for the shorter chronicity group and 0.09 ± 0.05, 0.15 ± 0.12, and 1.04 ± 0.15 for the longer chronicity group [Table 2]. The mean (±SD) Hmax/Mmax ratio, Hslp/Mslp, and Hth/Mth in the non-paretic legs were 0.26 ± 0.18, 0.48 ± 0.36, and 0.86 ± 0.14 for the shorter chronicity group and 0.26 ± 0.18, 0.5 ± 0.38, and 0.84 ± 0.15 for the longer chronicity group [Table 2].
Table 2: Electrophysiological data of the participants

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As motoneuron pool excitability was not significantly different between the shorter and longer chronicity groups, we performed the following analysis regardless of the time elapsed post-stroke. Both Hmax/Mmax and Hslp/Mslp were significantly higher on the paretic sides than on the non-paretic sides of the arms [Hmax/Mmax: 0.35 ± 0.31 vs. 0.10 ± 0.06, P < 0.001; Hslp/Mslp: 0.63 ± 0.51 vs. 0.19 ± 0.19, P < 0.001; [Figure 1]a and [Figure 1]c] and legs [Hmax/Mmax: 0.48 ± 0.35 vs. 0.26 ± 0.18, P < 0.001; Hslp/Mslp: 1.12 ± 0.90 vs. 0.50 ± 0.37; [Figure 1]b and [Figure 1]d]. Analysis of the Hth/Mth also showed a statistically smaller value in the paretic arms [0.91 ± 0.11 vs. 1.01 ± 0.18, P = 0.004; [Figure 1]e] when compared to the non-paretic sides post-stroke. However, no such difference was found in the paretic legs when compared with the non-paretic sides [0.82 ± 0.02 vs. 0.85 ± 0.02, P = 0.329; [Figure 1]f].
Figure 1: (a and b) Hslp/Mslp, (c and d) Hmax/Mmax, and (e and f) Hth/Mth ratios for both the unimpaired and spastic sides in the upper and lower limbs of stroke patients. Values are presented as mean ± standard deviation; ***P < 0.001 spastic side versus unimpaired side (Student's t-test).

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Comparison of the clinical evaluations of spasticity (modified Ashworth scale) and neurophysiological measurements

Next, we compared three neurophysiological parameters among individuals with different MAS scores. In either the upper or lower limbs, there were no significant differences in any of the three motoneuron pool excitability parameters, Hmax/Mmax ratio, Hslp/Mslp, and Hth/Mth, among patients with different MAS scores (all P > 0.05, data not shown). As the motoneuron pool excitability parameters in the non-paretic limbs differed among individuals, we further calculated the fold increase in the paretic side versus the non-paretic side for all three motor neuron pool excitability parameters. In the upper limbs, the Hslp/Mslp paretic/non-paretic ratio was significantly higher in patients with MAS scores of 2 and 3 than in those with MAS scores of 1 [MAS 2: 8.63 ± 7.31 vs. 2.73 ± 1.78; MAS 3: 11.79 ± 1.14 vs. 2.73 ± 1.78; both P < 0.05; [Figure 2]a] or MAS scores of 1+ [MAS 2: 8.63 ± 7.31 vs. 2.46 ± 1.46; MAS 3: 11.79 ± 1.14 vs. 2.46 ± 1.46; both P < 0.05; [Figure 2]a] there was a similar trend in the lower limbs. The Hslp/Mslp paretic/non-paretic ratio was significantly higher in patients with MAS scores of 2 and 3 when compared to those with MAS scores of 1 (MAS 1) [MAS 2: 6.08 ± 4.42 vs. 1.51 ± 0.64; MAS 3: 12.31 ± 3.95 vs. 1.51 ± 0.64; both P < 0.05; [Figure 2]b]. The Hslp/Mslp paretic/non-paretic ratio was also significantly higher in patients with MAS scores of 3 when compared to those with MAS scores of 1+ [12.31 ± 3.95 vs. 2.25 ± 1.49, P < 0.05; [Figure 2]b]. Likewise, compared with those with MAS 1, the patients with MAS 2 or MAS 3 had higher Hmax/Mmax paretic/non-paretic ratios in the upper limbs [MAS 2: 5.21 ± 3.49 vs. 2.62 ± 1.31; MAS 3: 9.90 ± 4.27 vs. 2.62 ± 1.31; both P < 0.05; [Figure 2]c]. However, the Hmax/Mmax paretic/non-paretic ratios did not differ significantly among patients with different lower limb MAS scores [all P > 0.05; [Figure 2]d]. Analysis of the Hth/Mth paretic/non-paretic ratio showed that the differences among different MAS groups were also not statistically significant in either the arms or legs [all P > 0.05; [Figure 2]e and [Figure 2]f].
Figure 2: Comparison of (a and b) the Hslp/Mslp paretic/non-paretic ratio, (c and d) the Hmax/Mmax paretic/non-paretic ratio, and (e and f) the Hth/Mth paretic/non-paretic ratio among different modified Ashworth scale groups. Values are presented as mean ± standard deviation; *P < 0.05 and **P < 0.01 versus the MAS 1 group; #P < 0.05 versus the MAS 1+ group (Kruskal–Wallis test).

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  Discussion Top


The major findings of this study were the following: (1) Both the Hmax/Mmax and Hslp/Mslp ratios were significantly higher in the spastic sides than in the unimpaired sides of the upper and lower limbs, whereas the Hth/Mth ratio showed significant differences only between the two sides of the upper limbs; (2) the Hslp/Mslp paretic/non-paretic ratio was increased in patients with MAS scores of 2 or 3 when compared to those with MAS 1 scores for the upper and lower limbs, whereas the Hmax/Mmax paretic/non-paretic ratio showed significant differences between MAS scores of 2 or 3 and 1 only in the upper limbs; and (3) in either spastic or unimpaired sides, there were no significant differences for all the three motoneuron pool excitability parameters, Hmax/Mmax, Hslp/Mslp and Hth/Mth, between the shorter chronicity (time post-stroke ≤6 months) and longer chronicity groups (time post-stroke >6 months) for both the upper and lower limbs.

In the current study, we found that motoneuron pool excitability, as measured using Hslp/Mslp and Hmax/Mmax, was significantly greater on the spastic side than on the unimpaired side in both upper and lower limbs, whereas Hth/Mth only revealed significant differences between the two sides of the upper limb. Moreover, we showed that the Hslp/Mslp paretic/non-paretic ratio was increased in patients with MAS scores of 2 or 3 when compared to those with MAS scores of 1 for both the upper and lower limbs. However, the Hmax/Mmax paretic/non-paretic ratios differed significantly among patients with different MAS scores only in the upper limbs. Our results support the findings from previous studies that used Hslp/Mslp instead of Hmax/Mmax and Hth/Mth to estimate spinal excitability in stroke patients.[10],[12],[21],[22]

As suggested by several authors,[9],[15],[23] the Hslp/Mslp ratio is the preferred index for assessing motor neuron pool excitability. This is because this index compares the ascending slope of the H response, where only reflexively activated motoneurons are responsive. In addition, there is no collision in the motor axons (since there are no M-waves present) nor in the ascending slope of the M-wave, where motoneurons are directly activated. One crucial problem with Hmax/Mmax is that a collision effect occurs between a descending H-reflex discharge and an ascending antidromic motor volley within the alpha motor axons as the stimulation intensity increases.[24] At low stimulation intensities, the Ia sensory fibers are selectively activated, yielding an H-reflex without the M potential. With increasing stimulation, more Ia sensory fibers are activated with larger H amplitudes, as are some of the motor fibers with small M amplitudes, which will cause a collision effect. The true maximum H-reflex amplitude could not be obtained, resulting in a relatively small Hmax/Mmax ratio. In contrast, the assessment of Hslp/Mslp minimized the effects of antidromic activity. In regards to the problem with the Hth/Mth ratio, it has been suggested that Hth is less sensitive to changes in the excitability of the motoneuron pool during additional facilitatory or inhibitory stimuli than Hmax.[24] Previous work has also shown that the degree of post-stroke spasticity correlates well with their Hslp/Mslp values, but not with Hmax/Mmax or Hth/Mth.[22] Our results support the recommendation of using Hslp/Mslp to estimate spinal excitability in both the upper and lower limbs of stroke patients.

While previous neurophysiological studies on post-stroke spasticity mainly focused almost exclusively on patients with chronic stroke,[10],[11],[12],[13],[17] the current study included patients with different durations post-stroke (≤6 months and >6 months). Although changes in neuronal plasticity after stroke may lead to high variability in the onset of post-stroke spasticity, the onset time of post-stroke spasticity is mostly within one month.[18] Our results based on chronicity showed that Hmax/Mmax, Hth/Mth, and Hslp/Mslp on both the paretic upper and lower limbs did not differ between the longer (mean 4.7 years) and shorter chronicity groups (mean 0.3 years). These findings are in agreement with those of a previous report showing that presynaptic inhibition of the FCR H-reflex was equally impaired in both acute (<3 months post-stroke) and chronic (>9 months post-stroke) stroke patients.[25] In parallel with the neurophysiological findings, a recent meta-analysis suggested that post-stroke spasticity usually appeared or disappeared within one to 3 months after stroke and remained stable beyond 3 months.[26] However, previous work testing the effect of chronicity revealed that the paretic arm Hslp/Mslp was significantly greater in the longer chronicity group (mean 9.4 years) than in the shorter chronicity group (mean 2.5 years).[10] Here, the mean post-stroke durations for the longer and shorter chronicity groups were 4.7 years and 0.3 years respectively, which were much shorter than those reported in the aforementioned study. It is possible that more chronic stroke patients may participate less actively in physical rehabilitation, which could increase their risk for spasticity and be responsible for the greater Hslp/Mslp values observed in the previous study. Nevertheless, our findings emphasize the importance of using Hslp/Mslp to evaluate the spasticity of stroke patients in both the subacute and chronic stages.

We found that in both the upper and lower limbs, there were no significant differences in Hslp/Mslp among patients with different MAS scores. However, in both the upper and lower limbs, the Hslp/Mslp paretic/non-paretic ratio was significantly higher in patients with MAS scores of 2 and 3 than in those with MAS scores of 1. While the intra-subject variability of the H-reflex is relatively small, it is known to vary widely between individuals.[27] Because of this variability, the Hslp/Mslp ratio between the spastic and unimpaired sides is a more useful indicator for comparing motoneuron pool excitability among individuals. In two of our 60 patients, lower limb H-reflexes could not be obtained on the unimpaired side. Absent H-reflexes in the unimpaired lower limbs of stroke patients have also been reported in previous studies.[22] Lack of muscle use due to secondary effects of stroke may contribute to decreased motor neuron excitability. Accumulating evidence has documented less ambulatory activity in patients with stroke than in healthy controls.[28],[29] Prolonged periods of muscle disuse would lower motoneuron excitability, resulting in lower H-reflex amplitudes.[30],[31],[32]

This study has some limitations that need to be addressed. This study examined the relationship between MAS and neurophysiological parameters in a moderate sample size (n = 60). The number of patients with each MAS score was insufficient. A larger sample size for every MAS score is needed to validate the neurophysiological parameters. We chose the MAS as the measurement tool for clinical spasticity because it is the most commonly used clinical tool for spasticity evaluation.[5] However, the reliability and sensitivity validity of the MAS are questionable, especially due to the ambiguity between grades of “1” and “1+”.[8] In addition, its insufficient sensitivity may cause most patients to be classified as having a moderate degree of the clustering effect.[8] Future research using other clinical scales, such as the modified MAS[33],[34] or modified Tardieu scale,[35],[36] should be considered.


  Conclusion Top


For patients with subacute and chronic stroke, measurement of Hslp/Mslp can provide additional neurophysiological information that is complementary to MAS scores in evaluating post-stroke spasticity. The Hslp/Mslp ratio was significantly greater on the spastic side than on the unimpaired side in both the upper and lower limbs. Moreover, in both the upper and lower limbs, the Hslp/Mslp ratio between the spastic side and the unimpaired side increased in patients with MAS scores of 2 or 3 as opposed to in those with MAS scores of 1. These results suggest that Hslp/Mslp could be a potential neurophysiological indicator for evaluating the degree of spasticity in both the upper and lower limbs of patients with hemiplegia.

Acknowledgment

The authors are grateful to the Taipei Common Laboratory of Chang Gung Memorial Hospital for providing statistical assistance.

Financial support and sponsorship

This work was supported by grants from the Cheng Hsin General Hospital (CHNDMC-110-8, CHNDMC-110-3 and CHNDMC-111-02).

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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