Authors: Chu-Hsu Lin, MD Kai-Hua Chen, MD Chia-Hao Chang, PhD Chien-Min Chen, MD Ying Chih Huang, MD Hung-Chih Hsu, MD Chang-Zern Hong, MD
Stroke
ORIGINAL RESEARCH ARTICLE
Affiliations: From the Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Yunlin, Taiwan (C-HL); Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Chiayi, Taiwan (K-HC, C-MC, H-CH); School of Medicine, Chang Gung University, Taoyuan, Taiwan (K-HC, C-MC); Department of Nursing, Chang Gung University of Science and Technology, Chiayi Campus, Chiayi, Taiwan (C-HC, H-CH); Department of Neurology, Chang Gung Memorial Hospital, Chiayi, Taiwan (YCH); Graduate Institute of Clinical Medical Sciences, College of Medicine, Chang Gung University, Taoyuan, Taiwan (H-CH); and Department of Physical Therapy, Hung Kuang University, Taichung County, Taiwan (C-ZH).
Correspondence: All correspondence and requests for reprints should be addressed to Hung-Chih Hsu, MD, Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Chiayi, No. 6, W. Sec., Jiapu Rd, Puzih City, Chiayi County 613, Taiwan, Republic of China.
Disclosures: Funded by Chang Gung Memorial Hospital (CMRPG680511, CMRPG680512). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
Muscle Pain Intensity and Pressure Pain Threshold Changes in Different Periods of Stroke Patients ABSTRACT Lin C-H, Chen K-H, Chang C-H, Chen C-M, Huang YC, Hsu H-C, Hong C-Z: Muscle pain intensity and pressure pain threshold changes in different periods of stroke patients. Am J Phys Med Rehabil 2014;93:299Y309.
Objective: This study aimed to investigate the role of muscle pain in poststroke pain syndromes.
Design: This cross-sectionalYdesigned study enrolled 145 stroke patients at three different stroke duration periods (e3 mos, 3 mos to 1 yr, and 91 yr) receiving inpatient or outpatient rehabilitation programs in a regional teaching hospital. Three common muscle tender points (two at the upper trapezius and one at the brachioradialis) and two relative periosteum points of the healthy and hemiparetic sides were identified for evaluation. Spontaneous pain intensity measured with the verbally reported numerical rating scale and pressure pain threshold were assessed. Associations between variables were analyzed.
Results: Among 145 subjects, 56 were women, and the mean T SD age was 62.1 T 13.2 yrs. The patients with stroke duration within 3 mos had the highest spontaneous muscle pain intensity and were most sensitive to pressure pain, with a prevalence of 48.3% of moderate to severe pain intensity (verbally reported numerical rating scale, 4Y10) in the hemiparetic side. Spontaneous pain was more severe in the hemiparetic side than in the healthy side, but there were no obvious differences between the sides in the pressure pain threshold of the muscle or the periosteum.
Conclusions: In stroke patients, spontaneous muscle pain in the hemiparetic 0894-9115/14/9304-0299 American Journal of Physical Medicine & Rehabilitation Copyright * 2013 by Lippincott Williams & Wilkins
side is a common finding. Bilaterally symmetric changes of pressure pain threshold are probably caused by central sensitization mechanisms. Key Words:
Stroke, Pain, Pressure Pain Threshold, Tender Point
DOI: 10.1097/PHM.0000000000000003
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S
MATERIALS AND METHODS
troke is a global health issue and the second most common cause of death worldwide.1 It is a major cause of long-term disability, resulting in considerable emotional stress and socioeconomic burden to the patients, their families, and the health service system.2 Pain is one of the most common complications after stroke, with prevalence reported to be from 19% to 74%.3Y9 However, it is often underrecognized and undertreated and often presents with an exceptionally complex nature. Some pain develops after stroke; some pain may actually occur before stroke but may also change in intensity after stroke.4 The mechanisms of poststroke pain are often multifactorial and composite. These underlying pathologies may present alone, or several pathologies may coexist. Each pathology may prompt the development of another one.9 Hemiparetic-side central post-stroke pain and regional shoulder pain such as rotator cuff tendon disorders and adhesive capsulitis have been addressed most often in previous studies, whereas other complications such as deep vein thrombosis or pressure ulcers may also be the source of pain.5,7,9,10 Muscle pain is a common origin of pain in clinical practice, and various etiologies can be responsible.11 Stroke-related hemiplegia or hemiparesis resulting in postural imbalance, muscle spasticity, weakness and overuse, and even emotional stress can possibly become the predisposing factors of muscle pain.11 However, to the authors_ knowledge, studies focused on post-stroke muscle pain are lacking.9 Subjective or spontaneous muscle pain and pressure pain threshold (PPT) are two important parameters in the research of muscle pain.11 The former directly represents the symptoms the patient usually experiences although it is relatively subjective. The latter represents the sensitivity to pain from compressions. Both parameters are associated with each other in previous reports, although the causal relationship is difficult to define.11Y13 Whether the hemiparetic-side weakness of the muscle or the hemiparetic-side damage to the central nervous system from stroke would cause changes in perception of spontaneous muscle pain or PPT between the healthy side and the hemiparetic side and whether these changes vary during the course of stroke are still unknown. Because the upper limb is reported to be the most common site of pain in stroke patients,4 the present study assessed the spontaneous muscle pain intensity and PPT of three common muscle tender points (MTePs) in the upper limb of stroke patients to investigate the possible roles of muscle pain in post-stroke pain syndromes.
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Study Design This cross-sectional study was designed to assess spontaneous pain intensity and the PPT of MTePs of the healthy and hemiparetic sides, as well as the PPT over bony prominences, for data normalization to abolish the central perceptual influence caused by stroke. This study was approved by the local institutional review board of Chiayi Chang Gung Memorial Hospital, a regional teaching hospital.
Subjects The present study enrolled first-ever hemiparetic stroke patients disregarding the type (ischemic or hemorrhagic) of the stroke. The lists of patients who had received regular inpatient or outpatient rehabilitation training programs in Chiayi Chang Gung Memorial Hospital, a regional teaching hospital, were reviewed per week by one physician of the Department of Physical Medicine and Rehabilitation. Patients who had stroke with bilateral sides involved such as brainstem stroke or with a history of previous stroke, traumatic brain injury, or other severe neuromuscular disorders other than this stroke; any ongoing disease; serious illness; trauma; limb deformities; and mental or cognitive deficit (including impaired consciousness, aphasia, dementia, or delirium) by medical records or found by contact with the subjects were excluded. Among the subjects enrolled, some received acute care for stroke in this regional teaching hospital but some did not. The former had brain computed tomographic imaging, and the diagnosis was confirmed by neurologists or neurosurgeons. The latter had official medical record summaries with stroke diagnosis for all patients, including the type and the onset of the stroke. Signed informed consents were obtained from all participants or their legal guardians after the study procedure was thoroughly explained. The subjects were divided into three groups according to time passed since the onset of stroke (e3 mos, 3 mos to 1 yr, and 91 yr). The medical records of all participants were reviewed, and baseline data, including age, sex, body height and weight, and main stroke type, were recorded. Motor function including the Brunnstrom stage and muscle power of the upper trapezius (testing the muscle power of shrugging the shoulders) and the brachioradialis (testing the muscle power of elbow flexion in neutral position between pronation and supination) were measured. The Brunnstrom stage was defined as I: flaccidity of the limbs, II:
Am. J. Phys. Med. Rehabil. & Vol. 93, No. 4, April 2014
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emergence of spasticity and synergies, III: voluntary movements in strong synergies, IV: movements deviating from basic synergies, V: relative independence of basic synergies, and IV: nearly normal motor control and coordination.14 Muscle power was measured with manual muscle tests based on 0Y5 grades (0: complete paralysis, 1: flicker of contraction present, 2: active movement with gravity eliminated, 3: active movement against gravity, 4: active movement against gravity and resistance, and 5: normal muscle power).
Procedure Identification of MTePs Three common MTePs of the upper trapezius and the brachioradialis were identified by finding the spot with most spontaneous pain at usual or most sensitivity to compression at the location described below. Firstly, the patient was asked: BDo you feel spontaneous pain at this area?[ BWhere? Which point?[ Then, gentle palpation was performed for confirmation. If the patient answered that there was no spontaneous pain at all, direct palpation at the region was performed to find the spot with most sensitivity to pressure pain. The locations of the three MTePs were the following: MTeP 1: Midportion of the anterior border of the upper trapezius. MTeP 2: Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. MTeP 3: In the center of the brachioradialis muscle belly, approximately one fingerbreadth below the antecubital fossa. After the MTePs were identified, these were marked for verbally reported numerical rating scale (VRS) and then PPT evaluations. The side (healthy side or hemiparetic) and the points of the muscle or the periosteum were all assessed in a randomized order by one trained research assistant.
Spontaneous Pain IntensityVVRS The patients were asked to report the current spontaneous pain intensity at the bilateral upper trapezius and brachioradialis MTePs as VRS scores ranging from 0 to 10, with 0 representing no pain and 10 representing the worst imaginable pain. VRS scores of 0, 1Y3, 4Y6, and 7Y10 points were defined as no pain, mild, moderate, and severe pain, respectively. www.ajpmr.com
Evaluation of the PPT A PPT meter, Force Dial FDK 20 with a steel rod covered by a rubber surface with an area of 1.0 cm 2 and a scale ranging from 0 to 10 kg (Wagner Instruments, Greenwich, CT), was used to measure PPT over the MTePs and the nearby periosteum. The procedures of PPT measurement as previously described by Fischer15 were applied in this study. The PPT was defined as the minimal pressure that caused the sensation change from pressure to pain. First, the procedures were explained clearly to the subject. The subject was in the sitting position, made comfortable, and encouraged to maintain complete relaxation. The MTePs of the upper trapezius and the brachioradialis and reference points at the acromion and the olecranon were identified and marked. The PPT meter was applied on the marked area with the metal rod perpendicular to the surface of the skin. The compression pressure was increased gradually at a speed of approximately 1 kg/sec. The subject was asked to say yes when he/she began to feel pain or discomfort, and the compression would stop immediately. If the subject demonstrated pain by pulling away or grimacing, which indicates that the pain threshold had been exceeded, he/she would be given instructions again and a repeat measurement would be taken to ensure that the Breal[ threshold is obtained. Three repetitive measurements at an interval of 20 secs were performed at each site, and the mean values of the three readings were used for analysis.
Statistical Analysis The Kolmogorov-Smirnov test was carried out to determine the distribution of the variables to decide whether a parametric test or a nonparametric test was used for statistical analysis. The Pearson W2, one-way analysis of variance, and Kruskal-Wallis or Mann-Whitney U tests were used to assess differences in variables between the different stroke duration period groups. For analysis, the possible factors affecting VRS or PPT and VRS or PPT differences between each categorical variable were analyzed with Mann-Whitney U tests, whereas the associations between the continuous or ordinal variables and VRS or PPT were analyzed with the Pearson or the Spearman correlation test. VRS or PPT between the healthy and hemiparetic sides and VRS or PPT among each of the tested points were compared using Wilcoxon_s signed-rank test. Because PPTs of MTePs or periosteum points were not normally distributed, the natural logarithmic value of PPT was used as the dependent variable in Muscle Pain in Patients With Stroke
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the multivariate linear regression to analyze the possible associated factors noted by univariate analysis, including age, sex, and stroke duration (with and without VRS) of each MTeP of the hemiparetic side. Stroke patients might have perceptual deficit (either hypoesthesia or hyperesthesia) in the hemiparetic side. Therefore, besides the PPT of each MTeP, the Bmuscle-periosteum PPT difference,[ which was calculated by subtracting the PPT of the MTeP from the PPT of the periosteum between the hemiparetic side and the healthy side, was also analyzed. BMuscle-periosteum PPT difference percentage[ was the percentage of the above value divided by the PPT of the periosteum. Statistical analyses were performed using the Statistical Package for the Social Sciences 12.0 software (Statistical Package for the Social Sciences Inc, Chicago, IL).
RESULTS Demographic and Clinical Data of Patients During a period of 1 yr 3 mos, a total of 145 subjects (56 women) with well documented, firstever hemiparetic stroke were included. Their mean T SD age was 62.1 T 13.2 yrs, ranging from 33 to 89 yrs. Among the subjects, 85 had experienced ischemic stroke and the others had experienced hemorrhagic stroke. The case numbers of Brunnstrom stages I, II, III, IV, V, and VI of the hemiparetic side were 8, 13, 41, 28, 15, and 40, respectively. The demographic and clinical data are shown in Table 1. In the subjects who had a stroke more than 1 yr ago, the mean age was the youngest, and there were more men and more patients with hemorrhagic stroke. However, no differences were seen in motor disabilities of the hemiparetic side between the groups of different stroke duration periods,
measured as the Brunnstrom stage or muscle power of the upper trapezius and the brachioradialis.
Spontaneous Pain Intensity of MTePs Figure 1 shows the mean VRS scores for MTeP 1, MTeP 2, and MTeP 3 in the healthy and hemiparetic sides. Ten subjects (6.9%) reported severe pain (VRS 7Y10) and 41 (28.3%) reported moderate pain (VRS: 4Y6) from at least one of the three MTePs in the hemiparetic side, whereas in the healthy side, only four (2.8%) reported severe pain and eight (5.5%) reported moderate pain. Fifty-two (35.9%) reported mild pain from at least one of the three MTePs and 42 (29.0%) reported no pain from all three MTePs in the hemiparetic side, whereas 50 (34.5%) reported mild pain and 83 (57.2%) reported no pain in the healthy side. The prevalence of moderate to severe spontaneous muscle pain from at least one of the three MTePs tested in the hemiparetic side decreased as the stroke duration increased, including 48.3%, 26.6%, and 25.4% for the subjects with stroke of 3 mos or less, 3 mos to 1 yr, and more than 1 yr, respectively. Table 2 shows spontaneous pain intensity of each MTeP in the healthy side and the hemiparetic side of the subjects with different stroke durations. The VRS scores at the MTePs of the hemiparetic side were higher than those of the healthy side despite different durations from onset of stroke. Besides, the pain intensity was highest in the subjects with stroke duration within 3 mos, followed by stroke duration of more than 1 yr and 3 mos to 1 yr. However, only the differences between the former two groups reached statistical significance in both the healthy and hemiparetic sides, although there was a trend toward higher VRS of the healthy side in the patients with stroke duration of more than 1 yr than in those with stroke duration of 3 mos to 1 yr.
TABLE 1 Demographic data of the subjects
Sex (female/male) Stroke type (ischemic/hemorrhagic) Age, mean T SD, yrs Brunnstrom stage, mean T SD Muscle power of trapezius, mean T SD Muscle power of brachioradialis, mean T SD
Stroke Duration: G3 mos
Stroke Duration: 3 mos È 1 yr
Stroke Duration: 91 yr
P
31/29 44/16
14/16 18/12
11/44 23/32
0.001a 0.003a
68.4 T 12.0 4.17 T 1.81 3.52 T 1.52
62.2 T 13.2 3.90 T 1.45 3.11 T 1.34
55.2 T 10.9 3.95 T 1.25 3.44 T 1.48
0.000b 0.922c 2.771c
2.87 T 1.71
2.52 T 1.91
2.36 T 1.80
2.347c
Determined by the Pearson W2 test. Determined by one-way analysis of variance. c Determined by the Kruskal-Wallis test. The P value is in bold if significant, i.e., P G 0.05. a b
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FIGURE 1 VRS at each MTeP in the healthy side and the hemiparetic side. The error bars represent one standard deviation. The P values were obtained by Wilcoxon_s signed-rank test to compare VRS between each MTePs. MTeP 1 indicates the midportion of the anterior border of the upper trapezius; MTeP 2, caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius; MTeP 3, at the center of the brachioradialis.
Factors Affecting VRS and PPT The female subjects had higher hemiparetic-side VRS scores than did the male subjects (P = 0.013, 0.026, and 0.053 for MTeP 1, MTeP 2, and MTeP 3, respectively) in the group of stroke duration within 3 mos. They also had lower PPT than did the male subjects in each MTeP or periosteum points in
both the healthy and hemiparetic sides (Table 3). The VRS at each MTeP of either the healthy or the hemiparetic side was highly associated with the VRS at the other MTeP in both the healthy and hemiparetic sides by correlation analysis (data not shown). It meant that if a side had higher VRS in one MTeP, it would also have higher VRS in the
TABLE 2 Spontaneous pain intensity of the healthy side and the hemiparetic side in subjects with different stroke durations Stroke Duration: G3 mos VRS (0Y10), Mean T SD MTeP 1d MTeP 2e f
MTeP 3
Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side
1.88 T 1.81 3.20 T 2.38 1.87 T 1.71 3.27 T 2.35 0.97 T 1.21 1.77 T 1.92
Pc 0.000 0.000 0.000
Stroke Duration: 3 mos È 1 yr VRS (0Y10), Mean T SD 0.33 T 1.47 T 0.33 T 1.73 T 0.00 T 0.80 T
0.18 1.96 0.18 2.16 0.00 1.58
Pc 0.001 0.001 0.017
Stroke Duration: 91 yr VRS (0Y10), Mean T SD 0.40 1.73 0.35 2.00 0.22 0.96
T 0.99 T 2.04 T 0.91 T 2.02 T 0.66 T 1.70
Pc
Pa
0.000 0.000 0.000 0.000 0.000 0.003 0.004 0.000 0.002
Pb 0.068 0.495 0.098 0.459 0.062 0.475
a Determined by the Mann-Whitney U test to compare VRS between two groups of subjects with different stroke durations (G3 mos vs. 91 yr). b Determined by the Mann-Whitney U test to compare VRS between two groups of subjects with different stroke durations (3 mos È 1 yr vs. 91 yr). c Determined by Wilcoxon_s signed-rank test to compare VRS of MTeP between the healthy and the hemiparetic side. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05.
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MTePs of the other sites. The older adult subjects seemed more sensitive to pressure pain, although the findings were not totally consistent (Table 3). Nevertheless, age was not associated with VRS scores, and stroke type (ischemic or hemorrhagic), Brunnstrom stage, and muscle power of the upper trapezius or the brachioradialis of the hemiparetic side was not associated with PPT or VRS at each MTeP (data not shown).
PPT at Each MTeP or Periosteum Point The PPT values for each muscle or periosteum point were obtained by the mean of the three repetitive measurements with an acceptable reliability (Cronbach_s > value ranging from 0.929 to 0.957 for each point). Figure 2 shows the mean PPT at each MTeP or periosteum point. It was higher in the periosteum point than in the MTeP and the PPT for each MTeP, in increasing order, MTeP 1, MTeP 3 and MTeP 2, regardless of the healthy side or the hemiparetic side. However, there were no obvious differences in the PPT of the muscle or periosteum points between the healthy side and the hemiparetic side except in the subjects within 3 mos of stroke, for whom there was a trend toward lower PPT of MTeP 3 in the healthy side than in the hemiparetic side (Table 4). On the other hand, the PPT was generally lowest in the muscle and periosteum points in the subjects within 3 mos of stroke and highest in the subjects with stroke duration of more than 1 yr.
Multivariate linear regression (independent variables including stroke duration, age, and sex) revealed that stroke duration of less than 3 mos and female sex (data not shown) had significantly lower PPT of each MTeP or periosteum point of either the healthy or the hemiparetic side compared with those with stroke duration of more than 3 mos and male sex, although the variable Bage[ was no longer significant in the multivariate analysis (data not shown). The PPT was also lower in the subjects with stroke duration of less than 1 yr at MTeP 1 of the hemiparetic side, MTeP 3, and the olecranon point of both the healthy and hemiparetic sides compared with those with stroke duration of more than 1 yr (Table 4).
Comparison of Muscle-Periosteum PPT Difference While using periosteum PPT as the reference, no significant differences were found in muscleperiosteum PPT difference or muscle-periosteum PPT difference in percentages between bilateral MTePs (Table 5). Even for the subjects with moderate to severe pain at the MTePs of the hemiparetic side, the PPT or muscle-periosteum PPT difference of each MTeP was symmetric between the healthy and hemiparetic sides.
Association Between VRS and PPT Table 6 shows that higher spontaneous pain intensity in the hemiparetic side was associated
TABLE 3 The association of sex, age, and PPT Sex Female PPT, Mean T SD, kg/cm2 MTeP 1d MTeP 2e MTeP 3f Acromion Olecranon
Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side
1.62 T 1.58 T 2.29 T 2.35 T 1.81 T 2.06 T 2.52 T 2.76 T 2.59 T 2.69 T
0.60 0.46 0.77 0.73 0.50 0.67 0.81 1.08 0.83 1.00
Age
Male PPT, Mean T SD, kg/cm2
Pa
rb
Pc
1.99 T 0.64 1.99 T 0.72 2.99 T 1.15 2.84 T 1.14 2.51 T 0.92 2.65 T 1.09 3.58 T 1.49 3.36 T 1.25 3.34 T 1.23 3.34 T 1.28
0.000 0.000 0.000 0.017 0.000 0.001 0.000 0.005 0.000 0.003
j0.22 j0.17 j0.09 j0.05 j0.20 j0.13 j0.04 j0.04 j0.14 j0.17
0.008 0.047 0.283 0.583 0.018 0.131 0.610 0.649 0.087 0.043
a
Determined by the Mann-Whitney U test. Correlation coefficient determined by the Pearson correlation test to analyze the correlation between age and PPT of each MTeP and periosteum point. c Determined by the Pearson correlation test. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05. b
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FIGURE 2 PPT of each MTeP or periosteum point. The error bars represent one standard deviation. The P values were obtained by Wilcoxon_s signed-rank test to compare PPT between each MTePs. MTeP 1 indicates the midportion of the anterior border of the upper trapezius; MTeP 2, caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius; MTeP 3, at the center of the brachioradialis; AC, acromion; OL, olecranon.
with lower PPT at several sites: the VRS at MTeP 1 in the hemiparetic side correlated negatively with the PPT at MTeP 1, MTeP 2, and MTeP 3 and the peri-
osteum points at the acromion and the olecranon in the hemiparetic side and MTeP 1 in the healthy side. The VRS at MTeP 2 in the hemiparetic side
TABLE 4 PPT in subjects with different durations of stroke Stroke Duration: G3 mos PPT, Mean T SD, kg/cm2 MTeP 1d
Healthy side Hemiparetic side MTeP 2e Healthy side Hemiparetic side MTeP 3f Healthy side Hemiparetic side Acromion Healthy side Hemiparetic side Olecranon Healthy side Hemiparetic side
1.63 T 0.53 1.63 T 0.57 2.45 T 1.02 2.37 T 0.81 1.92 T 0.57 2.06 T 0.72 2.80 T 1.07 2.78 T 1.06 2.59 T 0.80 2.60 T 0.83
Pc 0.741 0.659 0.075 0.592 0.868
Stroke Duration: 3 mos È 1 yr PPT, Mean T SD, kg/cm2 1.93 T 0.67 1.83 T 0.60 2.89 T 1.22 2.75 T 0.98 2.32 T 1.07 2.51 T 1.06 3.53 T 1.78 3.36 T 1.33 3.31 T 1.45 3.31 T 1.40
Pc 0.452 0.381 0.188 0.789 0.894
Stroke Duration: 91 yr PPT, Mean T SD, kg/cm2 2.04 2.06 2.92 2.91 2.55 2.77 3.37 3.38 3.40 3.50
T 0.69 T 0.72 T 0.98 T 1.20 T 0.86 T 1.09 T 1.33 T 1.24 T 1.15 T 1.31
Pc
Pa
0.446 0.005 0.011 0.589 0.011 0.014 0.146 0.002 0.001 0.823 0.010 0.007 0.458 0.001 0.001
Pb 0.100 0.028 0.203 0.106 0.013 0.012 0.519 0.173 0.039 0.025
a Determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each MTeP or periosteum point; independent variable: age, sex, and stroke duration of G3 mos or 93 mos). b Determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each MTeP or periosteum point; independent variable: age, sex, and stroke duration of G1 yr or 91 yr). c Determined by Wilcoxon_s signed-rank test to compare PPT of MTeP or periosteum point between the healthy and the hemiparetic side. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05.
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TABLE 5 Muscle-periosteum PPT difference of each MTeP Stroke Duration: G3 mos (kg/cm2)/(%), Mean T SD AC: MTeP 1c
Healthy side Hemiparetic side AC: MTeP 1c/AC Healthy side Hemiparetic side AC: MTeP 2d Healthy side Hemiparetic side AC: MTeP 2d/AC Healthy side Hemiparetic side OL: MTeP 3e Healthy side Hemiparetic side OL: MTeP 3e/OL Healthy side Hemiparetic side
1.17 T 0.73 1.15 T 0.79 0.38 T 0.17 0.38 T 0.15 0.36 T 0.65 0.41 T 0.72 0.10 T 0.19 0.11 T 0.20 0.68 T 0.58 0.54 T 0.52 0.24 T 0.17 0.20 T 0.18
P
Stroke Duration: 3 mos È 1 yr (kg/cm2)/(%), Mean T SD
b
0.935 0.561 0.815 0.848 0.165 0.193
1.60 T 1.54 T 0.40 T 0.42 T 0.64 T 0.62 T 0.13 T 0.15 T 1.00 T 0.80 T 0.28 T 0.21 T
1.49 1.10 0.16 0.16 1.41 0.92 0.20 0.21 0.75 0.93 0.15 0.23
P
Stroke Duration: 91 yr b
0.861 0.704 0.967 0.926 0.191 0.072
(kg/cm2)/(%), Mean T SD 1.33 T 1.11 1.32 T 0.77 0.36 T 0.17 0.37 T 0.13 0.44 T 0.10 0.47 T 0.75 0.10 T 0.19 0.12 T 0.20 0.85 T 0.68 0.73 T 0.84 0.23 T 0.14 0.19 T 0.19
Pb
Pa
0.776 0.364 0.247 0.738 0.196 0.402 0.766 0.520 0.638 0.639 0.606 0.710 0.708 0.125 0.356 0.392 0.255 0.848
a
Determined by the Kruskal-Wallis test to analyze whether there was any difference of muscle-periosteum PPT difference and muscle-periosteum PPT difference percentage among the subjects with different durations of stroke. b Determined by Wilcoxon_s signed-rank test to compare muscle-periosteum PPT difference and muscle-periosteum PPT difference percentage between the healthy and the hemiparetic side. c At the midportion of the anterior border of the upper trapezius. d Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. e At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05. AC indicates acromion; OL, olecranon.
correlated negatively with the PPT at MTeP 1, MTeP 2, and MTeP 3 (trend) and the periosteum points at the acromion and the olecranon (trend) in the hemiparetic side and MTeP 1 (trend) in the healthy side. In addition, the VRS at MTeP 3 in the hemiparetic side correlated negatively with the PPT at MTeP 1 (trend) and MTeP 3 and the periosteum point at the acromion in the hemiparetic side and MTeP 3 (trend) in the healthy side.
DISCUSSION Spontaneous Muscle Pain Intensity The spontaneous pain intensity of the upper extremity measured with VRS was higher in the hemiparetic side than in the healthy side, and it was highest during the first 3 mos of stroke in both the hemiparetic side and the healthy side compared with that in the longer stroke duration periods. These findings are in line with current evidence on hemiparetic pain after stroke.4,7Y9 However, a slight trend was noted toward increasing VRS of the healthy side of stroke patients with stroke duration of more than 1 yr compared with that of patients with stroke duration of 3 mos to 1 yr. This might be related to chronic overuse of the healthy side in compensation for dysfunction of the limbs of the hemiparetic side. The prevalence of moderate to severe pain from at least one of the three MTePs in the hemiparetic
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side was 48.3% in the subjects with stroke duration within 3 mos. Prevalence decreased to 26.6% and 25.4% for the subjects with stroke duration of 3 mos to 1 yr and more than 1 yr, respectively. This was in general agreement with previous studies that disclosed that both the prevalence of pain and the etiologies of pain related to the stroke itself decreased during the chronic period of stroke.4,7 Interestingly, in this study, the prevalence of moderate to severe pain of the three common MTePs in the neck and upper limb region during the chronic period of stroke was fairly close to that of two previous reports, although the study design was different among each study.4,16 In the study of Jonsson et al.,4 297 stroke survivors were included. The patients were assessed 4 mos and 16 mos after stroke, with prevalence of moderate to severe pain reported as 32% and 21%, respectively. Whereas in the study of Glader et al.,16 the prevalence of pain, without regard to the pain intensity, was reported as 20% in 3203 patients with stroke duration more than 2 yrs. This might be partly explained by the fact that most pain in stroke patients involves the head, the neck, and the upper limb.4,8
Pressure Pain Threshold Because possible sensory dysfunction in the hemiparetic side may cause PPT changes, besides the absolute PPTs of MTePs, the differences in PPTs
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a Unstandardized coefficient and P value determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each muscle or periosteum point; independent variable: age, sex, stroke duration G3 mos vs. 93 mos and VRS at each MP. b At the midportion of the anterior border of the upper trapezius. c Caudal and slightly lateral to MP1, in the middle of the more nearly horizontal fibers of the upper trapezius. d At the center of the brachioradialis. The P value is in bold if significant or in trend. MP indicates muscle point; AC, acromion; OL, olecranon.
0.965 0.713 0.126 0.012 0.093 0.211 j0.001 0.01 0.05 j0.04 j0.02 j0.02 0.374 0.457 0.746 0.001 0.003 0.008 j0.02 j0.02 0.01 j0.05 j0.04 j0.05 0.975 0.589 0.955 0.028 0.060 0.013 j0.001 0.01 0.002 j0.03 j0.03 j0.04 0.278 0.594 0.274 0.003 0.008 0.182 j0.03 j0.01 0.04 j0.04 j0.04 j0.02 0.560 0.776 0.709 0.002 0.018 0.052 j0.01 j0.01 0.01 j0.04 j0.029 j0.03 0.571 0.451 0.828 0.363 0.981 0.351 j0.01 j0.02 0.01 j0.01 0.000 j0.02 0.531 0.464 0.813 0.135 0.324 0.235 j0.01 j0.02 0.01 j0.02 j0.01 j0.02 0.286 0.321 0.190 0.119 0.450 0.090 j0.02 j0.02 j0.04 j0.02 j0.01 j0.02 0.224 0.244 0.576 0.116 0.224 0.568 j0.03 j0.03 0.02 j0.02 j0.02 j0.01 0.132 0.118 0.819 0.016 0.066 0.527
P B P B P B P B P B P B P B P B P B
j0.03 j0.03 j0.01 j0.03 j0.02 j0.01 MP1b MP2c MP3d MP1a MP2c MP3d Healthy side VRS at VRS at VRS at Hemiparetic VRS at VRS at side VRS at
Pa Ba
PPT at OL
a a
PPT at AC
a
PPT at MP3
a a
PPT at MP2
a a a a
PPT at AC
a a
PPT at MP3
a a
PPT at MP2
a a
PPT at MP1
a
PPT at OL
a
PPT at MP1
a
Hemiparetic Side Healthy Side TABLE 6 Association between spontaneous pain and PPT
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between ipsilateral MTePs and periostea (relative PPTs) were also analyzed to eliminate the influence of hemiparetic-side sensory deficit. However, both the absolute PPTs and the relative PPTs were not significantly different between the hemiparetic side and the healthy side, even in the subjects with moderate to severe spontaneous pain in the hemiparetic side. One unexpected finding was that there was a trend toward slightly decreased sensitivity to pressure pain in the brachioradialis muscle in the hemiparetic side. Nevertheless, this might be caused by post-stroke sensory deficit, which could involve the distal limb more than the proximal shoulder girdle. The PPT was lowest (most sensitive to pressure pain) during the first 3 mos of stroke duration in both the hemiparetic and healthy sides and successively increased as the stroke duration increased, although the difference between stroke duration of 3 mos to 1 yr and more than 1 yr was modest. Although PPT levels before stroke were not known and there was no healthy control group for comparison, the PPT values at the upper trapezius region in the present study were apparently lower than those reported from one recent PPT topography study in healthy young adults.17 Thus, the PPT was assumed to become lower after stroke and gradually returned to baseline along with the course of the stroke, which indicated the existence of post-stroke sensitization. This sensitization phenomenon leading to increased sensitivity to pressure pain was correlated with the VRS score in the hemiparetic side and was not limited to the MTeP with spontaneous pain itself and also spread to other muscles and periosteum points bilaterally, disregarding the hemiparetic-side involvement of the stroke (Table 6). The Bspreading[ of the sensitization was more diffusely triggered by the upper trapezius MTePs, possibly because of the higher spontaneous pain intensity that occurred in the upper trapezius than in the brachioradialis (Table 6). This phenomenon might be related to a so-called central or extrasegmental sensitization mechanism; it has also been found in other pain disorders such as carpal tunnel syndrome and shoulder impingement syndrome.12,13 For example, one may have pain syndrome in the shoulder, whereas the PPT level could also be reduced in the lower leg muscle.13 This might explain why central post-stroke pain or other pain syndromes could also involve the healthy side of stroke patients4,10 and partly explain why the subjects had higher spontaneous pain intensity in the hemiparetic side but had symmetric PPT in both sides in the present study. The sensitized pressure pain hyperalgesia might be secondary to nociceptive Muscle Pain in Patients With Stroke
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input from post-stroke hemiparetic pain, but other mechanisms such as brain damage from the stroke itself or an abnormality in muscle balance could also be contributive.
Sex and Age Influences on Pain Perception This study found that the female sex was more sensitive to pressure pain stimulation and was associated with higher VRS scores in the MTePs of the hemiparetic side during the first few months after stroke. These findings were consistent with current evidences that women have lower PPTs than men do18 and are more likely to have chronic pain syndrome or more severe pain intensity in both the stroke population and the general population.4,19 The associations between age and pain perception are inconsistent in previous studies.20 One study of pain prevalence of stroke reported that pain intensity was lower in older stroke patients.4 However, another study revealed no association between age and shoulder pain on the hemiparetic side.7 Age effect on pain perception varies from different pain stimuli. It is reported that older subjects are more sensitive to pressure pain but are less sensitive to heat pain, and there are no age-related changes from electrical-currentYinduced pain.20Y22 In this study, age was not associated with spontaneous muscle pain but was negatively correlated with PPT when analyzed by univariate analysis (Table 3), which indicates that older stroke patients are more sensitive to pressure pain, although it lost the statistical significance when analyzed by multivariate linear regression. This could possibly be explained by the fact that the age difference in the present study was not as distinct as in the study of Lautenbacher et al.,21 which enrolled 20 young subjects between the ages of 21 and 35 yrs (mean T SD age, 27.1 T 3.5 yrs) and 20 older subjects between the ages of 63 and 88 yrs (mean age, 71.6 T 5.9 yrs).
Characteristics of Spontaneous Pain and PPT Topography This study found that VRS scores and PPTs were significantly different among different MTePs. However, the rank orders of VRS scores and PPTs among each MTeP were different (VRS scores in decreasing order: MTeP 2, MTeP 1, and MTeP 3 vs. sensitivity to pressure pain in decreasing order: MTeP 1, MTeP 3, and MTeP 2). The finding of higher VRS scores noted in the upper trapezius than scores in the brachioradialis muscle was expected because the former would be more affected
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by nearby hemiparetic shoulder pain, a frequent problem in stroke patients.4,7,9 Furthermore, the PPTs were symmetric bilaterally, which was in agreement with a recent topographic study of PPT12,17 that revealed the characteristic distribution of PPTs. Meanwhile, the present study found that this symmetrically distributed topography seemed not to be changed by the existence of hemiparesis or hemiplegia through the central or the extrasegmental sensitization process mentioned above. However, a further study with a large sample size is needed for confirmation.
Limitations of This Study The present study has several limitations. Firstly, VRS or PPT data from the subjects before stroke were not available for comparison in this cross-sectional study. Despite obvious increased intensity of spontaneous muscle pain in the hemiparetic side than in the healthy side, the exact extent of intensity change after stroke or whether the pain existed before stroke could not be known. Similarly, PPT levels before stroke were not known, and there was also no healthy control group for comparison. The assumption for post-stroke sensitization was made from comparisons of the PPT values with those reported from the previous study.17 Secondly, patients with serious illness or cognitive deficit such as impaired consciousness and aphasia, which could cause difficulty in evaluation of the VRS or PPT, were excluded from this study. On the other hand, patients with minor dysfunction from stroke might not go to a rehabilitation center and would not be included in this study. This may result in selection bias with inclusion of patients with a smaller range of severity of stroke. Thus, the results could not be representative for all stroke patients. This might cause difficulty in determining the association between pain symptoms and motor deficit measured with muscle power or the Brunnstrom stage, as reported in a previous study that showed that hemiparetic-side shoulder pain was associated with the degree of arm weakness.7 Thirdly, because of the cross-sectional design of this study, the data of VRS or PPT for analysis were from each patient with different durations of stroke but not from the same patient in different temporal courses. The results were generalized by adjusting the possible confounding factors among each individual such as age and sex but not from longitudinal observation. Finally, no information was available about whether any analgesic or muscle relaxant drugs
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were given at the time of investigation, and data were lacking regarding location, size, or degree of the cerebrovascular event. A further study would be needed to include this information.
CONCLUSIONS Stroke patients have the highest spontaneous muscle pain intensity and are most sensitive to pressure pain within 3 mos of stroke. Spontaneous muscle pain is more severe in the hemiparetic side than in the healthy side, but no differences are seen in the PPT of the muscle or the periosteum between the two sides. Bilateral symmetric lowering of PPT associated with hemiparetic-side spontaneous muscle pain intensity is assumed to be caused by central sensitization. Further investigation is needed to clarify the underlying mechanism.
REFERENCES 1. Sarti C, Rastenyte D, Cepaitis Z, et al: International trends in mortality from stroke, 1968 to 1994. Stroke 2000;31:1588Y601
9. Kalichman L, Ratmansky M: Underlying pathology and associated factors of hemiplegic shoulder pain. Am J Phys Med Rehabil 2011;90:768Y80 10. Kumar B, Kalita J, Kumar G, et al: Central poststroke pain: A review of pathophysiology and treatment. Anesth Analg 2009;108:1645Y57 11. Buskila D: Muscle pain in rehabilitation. Am J Phys Med Rehabil 2012;91:1101Y3 12. Fernandez-de-las-Penas C, de la Llave-Rincon AI, Fernandez-Carnero J, et al: Bilateral widespread mechanical pain sensitivity in carpal tunnel syndrome: Evidence of central processing in unilateral neuropathy. Brain 2009;132:1472Y9 13. Hidalgo-Lozano A, Fernandez-de-las-Penas C, AlonsoBlanco C, et al: Muscle trigger points and pressure pain hyperalgesia in the shoulder muscles in patients with unilateral shoulder impingement: A blinded, controlled study. Exp Brain Res 2010;202: 915Y25 14. Brunnstrom S: Movement Therapy in Hemiplegia: A Neurophysiological Approach. Philadelphia, PA, Harper & Row, 1970 15. Fischer AA: Pressure algometry over normal muscles. Standard values, validity and reproducibility of pressure threshold. Pain 1987;30:115Y26
2. Feigin VL, Lawes CM, Bennett DA, et al: Stroke epidemiology: A review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol 2003;2:43Y53
16. Glader EL, Stegmayr B, Johansson L, et al: Differences in long-term outcome between patients treated in stroke units and in general wards: A 2-year followup of stroke patients in Sweden. Stroke 2001;32: 2124Y30
3. Dekker JH, Wagenaar RC, Lankhorst GJ, et al: The painful hemiplegic shoulder: Effects of intra-articular triamcinolone acetonide. Am J Phys Med Rehabil 1997;76:43Y8
17. Binderup AT, Arendt-Nielsen L, Madeleine P: Pressure pain sensitivity maps of the neck-shoulder and the low back regions in men and women. BMC Musculoskelet Disord 2010;11:234
4. Jonsson AC, Lindgren I, Hallstrom B, et al: Prevalence and intensity of pain after stroke: A population based study focusing on patients_ perspectives. J Neurol Neurosurg Psychiatry 2006;77:590Y5
18. Garcia E, Godoy-Izquierdo D, Godoy JF, et al: Gender differences in pressure pain threshold in a repeated measures assessment. Psychol Health Med 2007;12: 567Y79
5. Langhorne P, Stott DJ, Robertson L, et al: Medical complications after stroke: A multicenter study. Stroke 2000;31:1223Y9
19. Bergman S, Herrstrom P, Hogstrom K, et al: Chronic musculoskeletal pain, prevalence rates, and sociodemographic associations in a Swedish population study. J Rheumatol 2001;28:1369Y77
6. Andersen G, Vestergaard K, Ingeman-Nielsen M, et al: Incidence of central post-stroke pain. Pain 1995;61: 187Y93
20. Gibson SJ, Helme RD: Age-related differences in pain perception and report. Clin Geriatr Med 2001;17: 433Y56
7. Gamble GE, Barberan E, Laasch HU, et al: Poststroke shoulder pain: A prospective study of the association and risk factors in 152 patients from a consecutive cohort of 205 patients presenting with stroke. Eur J Pain 2002;6:467Y74
21. Lautenbacher S, Kunz M, Strate P, et al: Age effects on pain thresholds, temporal summation and spatial summation of heat and pressure pain. Pain 2005; 115:410Y8
8. Widar M, Samuelsson L, Karlsson-Tivenius S, et al: Long-term pain conditions after a stroke. J Rehabil Med 2002;34:165Y70
22. Pickering G, Jourdan D, Eschalier A, et al: Impact of age, gender and cognitive functioning on pain perception. Gerontology 2002;48:112Y8
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Stroke
ORIGINAL RESEARCH ARTICLE
Affiliations: From the Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Yunlin, Taiwan (C-HL); Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Chiayi, Taiwan (K-HC, C-MC, H-CH); School of Medicine, Chang Gung University, Taoyuan, Taiwan (K-HC, C-MC); Department of Nursing, Chang Gung University of Science and Technology, Chiayi Campus, Chiayi, Taiwan (C-HC, H-CH); Department of Neurology, Chang Gung Memorial Hospital, Chiayi, Taiwan (YCH); Graduate Institute of Clinical Medical Sciences, College of Medicine, Chang Gung University, Taoyuan, Taiwan (H-CH); and Department of Physical Therapy, Hung Kuang University, Taichung County, Taiwan (C-ZH).
Correspondence: All correspondence and requests for reprints should be addressed to Hung-Chih Hsu, MD, Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Chiayi, No. 6, W. Sec., Jiapu Rd, Puzih City, Chiayi County 613, Taiwan, Republic of China.
Disclosures: Funded by Chang Gung Memorial Hospital (CMRPG680511, CMRPG680512). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
Muscle Pain Intensity and Pressure Pain Threshold Changes in Different Periods of Stroke Patients ABSTRACT Lin C-H, Chen K-H, Chang C-H, Chen C-M, Huang YC, Hsu H-C, Hong C-Z: Muscle pain intensity and pressure pain threshold changes in different periods of stroke patients. Am J Phys Med Rehabil 2014;93:299Y309.
Objective: This study aimed to investigate the role of muscle pain in poststroke pain syndromes.
Design: This cross-sectionalYdesigned study enrolled 145 stroke patients at three different stroke duration periods (e3 mos, 3 mos to 1 yr, and 91 yr) receiving inpatient or outpatient rehabilitation programs in a regional teaching hospital. Three common muscle tender points (two at the upper trapezius and one at the brachioradialis) and two relative periosteum points of the healthy and hemiparetic sides were identified for evaluation. Spontaneous pain intensity measured with the verbally reported numerical rating scale and pressure pain threshold were assessed. Associations between variables were analyzed.
Results: Among 145 subjects, 56 were women, and the mean T SD age was 62.1 T 13.2 yrs. The patients with stroke duration within 3 mos had the highest spontaneous muscle pain intensity and were most sensitive to pressure pain, with a prevalence of 48.3% of moderate to severe pain intensity (verbally reported numerical rating scale, 4Y10) in the hemiparetic side. Spontaneous pain was more severe in the hemiparetic side than in the healthy side, but there were no obvious differences between the sides in the pressure pain threshold of the muscle or the periosteum.
Conclusions: In stroke patients, spontaneous muscle pain in the hemiparetic 0894-9115/14/9304-0299 American Journal of Physical Medicine & Rehabilitation Copyright * 2013 by Lippincott Williams & Wilkins
side is a common finding. Bilaterally symmetric changes of pressure pain threshold are probably caused by central sensitization mechanisms. Key Words:
Stroke, Pain, Pressure Pain Threshold, Tender Point
DOI: 10.1097/PHM.0000000000000003
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S
MATERIALS AND METHODS
troke is a global health issue and the second most common cause of death worldwide.1 It is a major cause of long-term disability, resulting in considerable emotional stress and socioeconomic burden to the patients, their families, and the health service system.2 Pain is one of the most common complications after stroke, with prevalence reported to be from 19% to 74%.3Y9 However, it is often underrecognized and undertreated and often presents with an exceptionally complex nature. Some pain develops after stroke; some pain may actually occur before stroke but may also change in intensity after stroke.4 The mechanisms of poststroke pain are often multifactorial and composite. These underlying pathologies may present alone, or several pathologies may coexist. Each pathology may prompt the development of another one.9 Hemiparetic-side central post-stroke pain and regional shoulder pain such as rotator cuff tendon disorders and adhesive capsulitis have been addressed most often in previous studies, whereas other complications such as deep vein thrombosis or pressure ulcers may also be the source of pain.5,7,9,10 Muscle pain is a common origin of pain in clinical practice, and various etiologies can be responsible.11 Stroke-related hemiplegia or hemiparesis resulting in postural imbalance, muscle spasticity, weakness and overuse, and even emotional stress can possibly become the predisposing factors of muscle pain.11 However, to the authors_ knowledge, studies focused on post-stroke muscle pain are lacking.9 Subjective or spontaneous muscle pain and pressure pain threshold (PPT) are two important parameters in the research of muscle pain.11 The former directly represents the symptoms the patient usually experiences although it is relatively subjective. The latter represents the sensitivity to pain from compressions. Both parameters are associated with each other in previous reports, although the causal relationship is difficult to define.11Y13 Whether the hemiparetic-side weakness of the muscle or the hemiparetic-side damage to the central nervous system from stroke would cause changes in perception of spontaneous muscle pain or PPT between the healthy side and the hemiparetic side and whether these changes vary during the course of stroke are still unknown. Because the upper limb is reported to be the most common site of pain in stroke patients,4 the present study assessed the spontaneous muscle pain intensity and PPT of three common muscle tender points (MTePs) in the upper limb of stroke patients to investigate the possible roles of muscle pain in post-stroke pain syndromes.
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Study Design This cross-sectional study was designed to assess spontaneous pain intensity and the PPT of MTePs of the healthy and hemiparetic sides, as well as the PPT over bony prominences, for data normalization to abolish the central perceptual influence caused by stroke. This study was approved by the local institutional review board of Chiayi Chang Gung Memorial Hospital, a regional teaching hospital.
Subjects The present study enrolled first-ever hemiparetic stroke patients disregarding the type (ischemic or hemorrhagic) of the stroke. The lists of patients who had received regular inpatient or outpatient rehabilitation training programs in Chiayi Chang Gung Memorial Hospital, a regional teaching hospital, were reviewed per week by one physician of the Department of Physical Medicine and Rehabilitation. Patients who had stroke with bilateral sides involved such as brainstem stroke or with a history of previous stroke, traumatic brain injury, or other severe neuromuscular disorders other than this stroke; any ongoing disease; serious illness; trauma; limb deformities; and mental or cognitive deficit (including impaired consciousness, aphasia, dementia, or delirium) by medical records or found by contact with the subjects were excluded. Among the subjects enrolled, some received acute care for stroke in this regional teaching hospital but some did not. The former had brain computed tomographic imaging, and the diagnosis was confirmed by neurologists or neurosurgeons. The latter had official medical record summaries with stroke diagnosis for all patients, including the type and the onset of the stroke. Signed informed consents were obtained from all participants or their legal guardians after the study procedure was thoroughly explained. The subjects were divided into three groups according to time passed since the onset of stroke (e3 mos, 3 mos to 1 yr, and 91 yr). The medical records of all participants were reviewed, and baseline data, including age, sex, body height and weight, and main stroke type, were recorded. Motor function including the Brunnstrom stage and muscle power of the upper trapezius (testing the muscle power of shrugging the shoulders) and the brachioradialis (testing the muscle power of elbow flexion in neutral position between pronation and supination) were measured. The Brunnstrom stage was defined as I: flaccidity of the limbs, II:
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emergence of spasticity and synergies, III: voluntary movements in strong synergies, IV: movements deviating from basic synergies, V: relative independence of basic synergies, and IV: nearly normal motor control and coordination.14 Muscle power was measured with manual muscle tests based on 0Y5 grades (0: complete paralysis, 1: flicker of contraction present, 2: active movement with gravity eliminated, 3: active movement against gravity, 4: active movement against gravity and resistance, and 5: normal muscle power).
Procedure Identification of MTePs Three common MTePs of the upper trapezius and the brachioradialis were identified by finding the spot with most spontaneous pain at usual or most sensitivity to compression at the location described below. Firstly, the patient was asked: BDo you feel spontaneous pain at this area?[ BWhere? Which point?[ Then, gentle palpation was performed for confirmation. If the patient answered that there was no spontaneous pain at all, direct palpation at the region was performed to find the spot with most sensitivity to pressure pain. The locations of the three MTePs were the following: MTeP 1: Midportion of the anterior border of the upper trapezius. MTeP 2: Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. MTeP 3: In the center of the brachioradialis muscle belly, approximately one fingerbreadth below the antecubital fossa. After the MTePs were identified, these were marked for verbally reported numerical rating scale (VRS) and then PPT evaluations. The side (healthy side or hemiparetic) and the points of the muscle or the periosteum were all assessed in a randomized order by one trained research assistant.
Spontaneous Pain IntensityVVRS The patients were asked to report the current spontaneous pain intensity at the bilateral upper trapezius and brachioradialis MTePs as VRS scores ranging from 0 to 10, with 0 representing no pain and 10 representing the worst imaginable pain. VRS scores of 0, 1Y3, 4Y6, and 7Y10 points were defined as no pain, mild, moderate, and severe pain, respectively. www.ajpmr.com
Evaluation of the PPT A PPT meter, Force Dial FDK 20 with a steel rod covered by a rubber surface with an area of 1.0 cm 2 and a scale ranging from 0 to 10 kg (Wagner Instruments, Greenwich, CT), was used to measure PPT over the MTePs and the nearby periosteum. The procedures of PPT measurement as previously described by Fischer15 were applied in this study. The PPT was defined as the minimal pressure that caused the sensation change from pressure to pain. First, the procedures were explained clearly to the subject. The subject was in the sitting position, made comfortable, and encouraged to maintain complete relaxation. The MTePs of the upper trapezius and the brachioradialis and reference points at the acromion and the olecranon were identified and marked. The PPT meter was applied on the marked area with the metal rod perpendicular to the surface of the skin. The compression pressure was increased gradually at a speed of approximately 1 kg/sec. The subject was asked to say yes when he/she began to feel pain or discomfort, and the compression would stop immediately. If the subject demonstrated pain by pulling away or grimacing, which indicates that the pain threshold had been exceeded, he/she would be given instructions again and a repeat measurement would be taken to ensure that the Breal[ threshold is obtained. Three repetitive measurements at an interval of 20 secs were performed at each site, and the mean values of the three readings were used for analysis.
Statistical Analysis The Kolmogorov-Smirnov test was carried out to determine the distribution of the variables to decide whether a parametric test or a nonparametric test was used for statistical analysis. The Pearson W2, one-way analysis of variance, and Kruskal-Wallis or Mann-Whitney U tests were used to assess differences in variables between the different stroke duration period groups. For analysis, the possible factors affecting VRS or PPT and VRS or PPT differences between each categorical variable were analyzed with Mann-Whitney U tests, whereas the associations between the continuous or ordinal variables and VRS or PPT were analyzed with the Pearson or the Spearman correlation test. VRS or PPT between the healthy and hemiparetic sides and VRS or PPT among each of the tested points were compared using Wilcoxon_s signed-rank test. Because PPTs of MTePs or periosteum points were not normally distributed, the natural logarithmic value of PPT was used as the dependent variable in Muscle Pain in Patients With Stroke
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the multivariate linear regression to analyze the possible associated factors noted by univariate analysis, including age, sex, and stroke duration (with and without VRS) of each MTeP of the hemiparetic side. Stroke patients might have perceptual deficit (either hypoesthesia or hyperesthesia) in the hemiparetic side. Therefore, besides the PPT of each MTeP, the Bmuscle-periosteum PPT difference,[ which was calculated by subtracting the PPT of the MTeP from the PPT of the periosteum between the hemiparetic side and the healthy side, was also analyzed. BMuscle-periosteum PPT difference percentage[ was the percentage of the above value divided by the PPT of the periosteum. Statistical analyses were performed using the Statistical Package for the Social Sciences 12.0 software (Statistical Package for the Social Sciences Inc, Chicago, IL).
RESULTS Demographic and Clinical Data of Patients During a period of 1 yr 3 mos, a total of 145 subjects (56 women) with well documented, firstever hemiparetic stroke were included. Their mean T SD age was 62.1 T 13.2 yrs, ranging from 33 to 89 yrs. Among the subjects, 85 had experienced ischemic stroke and the others had experienced hemorrhagic stroke. The case numbers of Brunnstrom stages I, II, III, IV, V, and VI of the hemiparetic side were 8, 13, 41, 28, 15, and 40, respectively. The demographic and clinical data are shown in Table 1. In the subjects who had a stroke more than 1 yr ago, the mean age was the youngest, and there were more men and more patients with hemorrhagic stroke. However, no differences were seen in motor disabilities of the hemiparetic side between the groups of different stroke duration periods,
measured as the Brunnstrom stage or muscle power of the upper trapezius and the brachioradialis.
Spontaneous Pain Intensity of MTePs Figure 1 shows the mean VRS scores for MTeP 1, MTeP 2, and MTeP 3 in the healthy and hemiparetic sides. Ten subjects (6.9%) reported severe pain (VRS 7Y10) and 41 (28.3%) reported moderate pain (VRS: 4Y6) from at least one of the three MTePs in the hemiparetic side, whereas in the healthy side, only four (2.8%) reported severe pain and eight (5.5%) reported moderate pain. Fifty-two (35.9%) reported mild pain from at least one of the three MTePs and 42 (29.0%) reported no pain from all three MTePs in the hemiparetic side, whereas 50 (34.5%) reported mild pain and 83 (57.2%) reported no pain in the healthy side. The prevalence of moderate to severe spontaneous muscle pain from at least one of the three MTePs tested in the hemiparetic side decreased as the stroke duration increased, including 48.3%, 26.6%, and 25.4% for the subjects with stroke of 3 mos or less, 3 mos to 1 yr, and more than 1 yr, respectively. Table 2 shows spontaneous pain intensity of each MTeP in the healthy side and the hemiparetic side of the subjects with different stroke durations. The VRS scores at the MTePs of the hemiparetic side were higher than those of the healthy side despite different durations from onset of stroke. Besides, the pain intensity was highest in the subjects with stroke duration within 3 mos, followed by stroke duration of more than 1 yr and 3 mos to 1 yr. However, only the differences between the former two groups reached statistical significance in both the healthy and hemiparetic sides, although there was a trend toward higher VRS of the healthy side in the patients with stroke duration of more than 1 yr than in those with stroke duration of 3 mos to 1 yr.
TABLE 1 Demographic data of the subjects
Sex (female/male) Stroke type (ischemic/hemorrhagic) Age, mean T SD, yrs Brunnstrom stage, mean T SD Muscle power of trapezius, mean T SD Muscle power of brachioradialis, mean T SD
Stroke Duration: G3 mos
Stroke Duration: 3 mos È 1 yr
Stroke Duration: 91 yr
P
31/29 44/16
14/16 18/12
11/44 23/32
0.001a 0.003a
68.4 T 12.0 4.17 T 1.81 3.52 T 1.52
62.2 T 13.2 3.90 T 1.45 3.11 T 1.34
55.2 T 10.9 3.95 T 1.25 3.44 T 1.48
0.000b 0.922c 2.771c
2.87 T 1.71
2.52 T 1.91
2.36 T 1.80
2.347c
Determined by the Pearson W2 test. Determined by one-way analysis of variance. c Determined by the Kruskal-Wallis test. The P value is in bold if significant, i.e., P G 0.05. a b
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FIGURE 1 VRS at each MTeP in the healthy side and the hemiparetic side. The error bars represent one standard deviation. The P values were obtained by Wilcoxon_s signed-rank test to compare VRS between each MTePs. MTeP 1 indicates the midportion of the anterior border of the upper trapezius; MTeP 2, caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius; MTeP 3, at the center of the brachioradialis.
Factors Affecting VRS and PPT The female subjects had higher hemiparetic-side VRS scores than did the male subjects (P = 0.013, 0.026, and 0.053 for MTeP 1, MTeP 2, and MTeP 3, respectively) in the group of stroke duration within 3 mos. They also had lower PPT than did the male subjects in each MTeP or periosteum points in
both the healthy and hemiparetic sides (Table 3). The VRS at each MTeP of either the healthy or the hemiparetic side was highly associated with the VRS at the other MTeP in both the healthy and hemiparetic sides by correlation analysis (data not shown). It meant that if a side had higher VRS in one MTeP, it would also have higher VRS in the
TABLE 2 Spontaneous pain intensity of the healthy side and the hemiparetic side in subjects with different stroke durations Stroke Duration: G3 mos VRS (0Y10), Mean T SD MTeP 1d MTeP 2e f
MTeP 3
Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side
1.88 T 1.81 3.20 T 2.38 1.87 T 1.71 3.27 T 2.35 0.97 T 1.21 1.77 T 1.92
Pc 0.000 0.000 0.000
Stroke Duration: 3 mos È 1 yr VRS (0Y10), Mean T SD 0.33 T 1.47 T 0.33 T 1.73 T 0.00 T 0.80 T
0.18 1.96 0.18 2.16 0.00 1.58
Pc 0.001 0.001 0.017
Stroke Duration: 91 yr VRS (0Y10), Mean T SD 0.40 1.73 0.35 2.00 0.22 0.96
T 0.99 T 2.04 T 0.91 T 2.02 T 0.66 T 1.70
Pc
Pa
0.000 0.000 0.000 0.000 0.000 0.003 0.004 0.000 0.002
Pb 0.068 0.495 0.098 0.459 0.062 0.475
a Determined by the Mann-Whitney U test to compare VRS between two groups of subjects with different stroke durations (G3 mos vs. 91 yr). b Determined by the Mann-Whitney U test to compare VRS between two groups of subjects with different stroke durations (3 mos È 1 yr vs. 91 yr). c Determined by Wilcoxon_s signed-rank test to compare VRS of MTeP between the healthy and the hemiparetic side. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05.
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MTePs of the other sites. The older adult subjects seemed more sensitive to pressure pain, although the findings were not totally consistent (Table 3). Nevertheless, age was not associated with VRS scores, and stroke type (ischemic or hemorrhagic), Brunnstrom stage, and muscle power of the upper trapezius or the brachioradialis of the hemiparetic side was not associated with PPT or VRS at each MTeP (data not shown).
PPT at Each MTeP or Periosteum Point The PPT values for each muscle or periosteum point were obtained by the mean of the three repetitive measurements with an acceptable reliability (Cronbach_s > value ranging from 0.929 to 0.957 for each point). Figure 2 shows the mean PPT at each MTeP or periosteum point. It was higher in the periosteum point than in the MTeP and the PPT for each MTeP, in increasing order, MTeP 1, MTeP 3 and MTeP 2, regardless of the healthy side or the hemiparetic side. However, there were no obvious differences in the PPT of the muscle or periosteum points between the healthy side and the hemiparetic side except in the subjects within 3 mos of stroke, for whom there was a trend toward lower PPT of MTeP 3 in the healthy side than in the hemiparetic side (Table 4). On the other hand, the PPT was generally lowest in the muscle and periosteum points in the subjects within 3 mos of stroke and highest in the subjects with stroke duration of more than 1 yr.
Multivariate linear regression (independent variables including stroke duration, age, and sex) revealed that stroke duration of less than 3 mos and female sex (data not shown) had significantly lower PPT of each MTeP or periosteum point of either the healthy or the hemiparetic side compared with those with stroke duration of more than 3 mos and male sex, although the variable Bage[ was no longer significant in the multivariate analysis (data not shown). The PPT was also lower in the subjects with stroke duration of less than 1 yr at MTeP 1 of the hemiparetic side, MTeP 3, and the olecranon point of both the healthy and hemiparetic sides compared with those with stroke duration of more than 1 yr (Table 4).
Comparison of Muscle-Periosteum PPT Difference While using periosteum PPT as the reference, no significant differences were found in muscleperiosteum PPT difference or muscle-periosteum PPT difference in percentages between bilateral MTePs (Table 5). Even for the subjects with moderate to severe pain at the MTePs of the hemiparetic side, the PPT or muscle-periosteum PPT difference of each MTeP was symmetric between the healthy and hemiparetic sides.
Association Between VRS and PPT Table 6 shows that higher spontaneous pain intensity in the hemiparetic side was associated
TABLE 3 The association of sex, age, and PPT Sex Female PPT, Mean T SD, kg/cm2 MTeP 1d MTeP 2e MTeP 3f Acromion Olecranon
Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side Healthy side Hemiparetic side
1.62 T 1.58 T 2.29 T 2.35 T 1.81 T 2.06 T 2.52 T 2.76 T 2.59 T 2.69 T
0.60 0.46 0.77 0.73 0.50 0.67 0.81 1.08 0.83 1.00
Age
Male PPT, Mean T SD, kg/cm2
Pa
rb
Pc
1.99 T 0.64 1.99 T 0.72 2.99 T 1.15 2.84 T 1.14 2.51 T 0.92 2.65 T 1.09 3.58 T 1.49 3.36 T 1.25 3.34 T 1.23 3.34 T 1.28
0.000 0.000 0.000 0.017 0.000 0.001 0.000 0.005 0.000 0.003
j0.22 j0.17 j0.09 j0.05 j0.20 j0.13 j0.04 j0.04 j0.14 j0.17
0.008 0.047 0.283 0.583 0.018 0.131 0.610 0.649 0.087 0.043
a
Determined by the Mann-Whitney U test. Correlation coefficient determined by the Pearson correlation test to analyze the correlation between age and PPT of each MTeP and periosteum point. c Determined by the Pearson correlation test. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05. b
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FIGURE 2 PPT of each MTeP or periosteum point. The error bars represent one standard deviation. The P values were obtained by Wilcoxon_s signed-rank test to compare PPT between each MTePs. MTeP 1 indicates the midportion of the anterior border of the upper trapezius; MTeP 2, caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius; MTeP 3, at the center of the brachioradialis; AC, acromion; OL, olecranon.
with lower PPT at several sites: the VRS at MTeP 1 in the hemiparetic side correlated negatively with the PPT at MTeP 1, MTeP 2, and MTeP 3 and the peri-
osteum points at the acromion and the olecranon in the hemiparetic side and MTeP 1 in the healthy side. The VRS at MTeP 2 in the hemiparetic side
TABLE 4 PPT in subjects with different durations of stroke Stroke Duration: G3 mos PPT, Mean T SD, kg/cm2 MTeP 1d
Healthy side Hemiparetic side MTeP 2e Healthy side Hemiparetic side MTeP 3f Healthy side Hemiparetic side Acromion Healthy side Hemiparetic side Olecranon Healthy side Hemiparetic side
1.63 T 0.53 1.63 T 0.57 2.45 T 1.02 2.37 T 0.81 1.92 T 0.57 2.06 T 0.72 2.80 T 1.07 2.78 T 1.06 2.59 T 0.80 2.60 T 0.83
Pc 0.741 0.659 0.075 0.592 0.868
Stroke Duration: 3 mos È 1 yr PPT, Mean T SD, kg/cm2 1.93 T 0.67 1.83 T 0.60 2.89 T 1.22 2.75 T 0.98 2.32 T 1.07 2.51 T 1.06 3.53 T 1.78 3.36 T 1.33 3.31 T 1.45 3.31 T 1.40
Pc 0.452 0.381 0.188 0.789 0.894
Stroke Duration: 91 yr PPT, Mean T SD, kg/cm2 2.04 2.06 2.92 2.91 2.55 2.77 3.37 3.38 3.40 3.50
T 0.69 T 0.72 T 0.98 T 1.20 T 0.86 T 1.09 T 1.33 T 1.24 T 1.15 T 1.31
Pc
Pa
0.446 0.005 0.011 0.589 0.011 0.014 0.146 0.002 0.001 0.823 0.010 0.007 0.458 0.001 0.001
Pb 0.100 0.028 0.203 0.106 0.013 0.012 0.519 0.173 0.039 0.025
a Determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each MTeP or periosteum point; independent variable: age, sex, and stroke duration of G3 mos or 93 mos). b Determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each MTeP or periosteum point; independent variable: age, sex, and stroke duration of G1 yr or 91 yr). c Determined by Wilcoxon_s signed-rank test to compare PPT of MTeP or periosteum point between the healthy and the hemiparetic side. d At the midportion of the anterior border of the upper trapezius. e Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. f At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05.
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TABLE 5 Muscle-periosteum PPT difference of each MTeP Stroke Duration: G3 mos (kg/cm2)/(%), Mean T SD AC: MTeP 1c
Healthy side Hemiparetic side AC: MTeP 1c/AC Healthy side Hemiparetic side AC: MTeP 2d Healthy side Hemiparetic side AC: MTeP 2d/AC Healthy side Hemiparetic side OL: MTeP 3e Healthy side Hemiparetic side OL: MTeP 3e/OL Healthy side Hemiparetic side
1.17 T 0.73 1.15 T 0.79 0.38 T 0.17 0.38 T 0.15 0.36 T 0.65 0.41 T 0.72 0.10 T 0.19 0.11 T 0.20 0.68 T 0.58 0.54 T 0.52 0.24 T 0.17 0.20 T 0.18
P
Stroke Duration: 3 mos È 1 yr (kg/cm2)/(%), Mean T SD
b
0.935 0.561 0.815 0.848 0.165 0.193
1.60 T 1.54 T 0.40 T 0.42 T 0.64 T 0.62 T 0.13 T 0.15 T 1.00 T 0.80 T 0.28 T 0.21 T
1.49 1.10 0.16 0.16 1.41 0.92 0.20 0.21 0.75 0.93 0.15 0.23
P
Stroke Duration: 91 yr b
0.861 0.704 0.967 0.926 0.191 0.072
(kg/cm2)/(%), Mean T SD 1.33 T 1.11 1.32 T 0.77 0.36 T 0.17 0.37 T 0.13 0.44 T 0.10 0.47 T 0.75 0.10 T 0.19 0.12 T 0.20 0.85 T 0.68 0.73 T 0.84 0.23 T 0.14 0.19 T 0.19
Pb
Pa
0.776 0.364 0.247 0.738 0.196 0.402 0.766 0.520 0.638 0.639 0.606 0.710 0.708 0.125 0.356 0.392 0.255 0.848
a
Determined by the Kruskal-Wallis test to analyze whether there was any difference of muscle-periosteum PPT difference and muscle-periosteum PPT difference percentage among the subjects with different durations of stroke. b Determined by Wilcoxon_s signed-rank test to compare muscle-periosteum PPT difference and muscle-periosteum PPT difference percentage between the healthy and the hemiparetic side. c At the midportion of the anterior border of the upper trapezius. d Caudal and slightly lateral to MTeP 1, in the middle of the more nearly horizontal fibers of the upper trapezius. e At the center of the brachioradialis. The P value is in bold if significant, i.e., P G 0.05. AC indicates acromion; OL, olecranon.
correlated negatively with the PPT at MTeP 1, MTeP 2, and MTeP 3 (trend) and the periosteum points at the acromion and the olecranon (trend) in the hemiparetic side and MTeP 1 (trend) in the healthy side. In addition, the VRS at MTeP 3 in the hemiparetic side correlated negatively with the PPT at MTeP 1 (trend) and MTeP 3 and the periosteum point at the acromion in the hemiparetic side and MTeP 3 (trend) in the healthy side.
DISCUSSION Spontaneous Muscle Pain Intensity The spontaneous pain intensity of the upper extremity measured with VRS was higher in the hemiparetic side than in the healthy side, and it was highest during the first 3 mos of stroke in both the hemiparetic side and the healthy side compared with that in the longer stroke duration periods. These findings are in line with current evidence on hemiparetic pain after stroke.4,7Y9 However, a slight trend was noted toward increasing VRS of the healthy side of stroke patients with stroke duration of more than 1 yr compared with that of patients with stroke duration of 3 mos to 1 yr. This might be related to chronic overuse of the healthy side in compensation for dysfunction of the limbs of the hemiparetic side. The prevalence of moderate to severe pain from at least one of the three MTePs in the hemiparetic
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side was 48.3% in the subjects with stroke duration within 3 mos. Prevalence decreased to 26.6% and 25.4% for the subjects with stroke duration of 3 mos to 1 yr and more than 1 yr, respectively. This was in general agreement with previous studies that disclosed that both the prevalence of pain and the etiologies of pain related to the stroke itself decreased during the chronic period of stroke.4,7 Interestingly, in this study, the prevalence of moderate to severe pain of the three common MTePs in the neck and upper limb region during the chronic period of stroke was fairly close to that of two previous reports, although the study design was different among each study.4,16 In the study of Jonsson et al.,4 297 stroke survivors were included. The patients were assessed 4 mos and 16 mos after stroke, with prevalence of moderate to severe pain reported as 32% and 21%, respectively. Whereas in the study of Glader et al.,16 the prevalence of pain, without regard to the pain intensity, was reported as 20% in 3203 patients with stroke duration more than 2 yrs. This might be partly explained by the fact that most pain in stroke patients involves the head, the neck, and the upper limb.4,8
Pressure Pain Threshold Because possible sensory dysfunction in the hemiparetic side may cause PPT changes, besides the absolute PPTs of MTePs, the differences in PPTs
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a Unstandardized coefficient and P value determined by multivariate linear regression (dependent variable: natural logarithm of PPT of each muscle or periosteum point; independent variable: age, sex, stroke duration G3 mos vs. 93 mos and VRS at each MP. b At the midportion of the anterior border of the upper trapezius. c Caudal and slightly lateral to MP1, in the middle of the more nearly horizontal fibers of the upper trapezius. d At the center of the brachioradialis. The P value is in bold if significant or in trend. MP indicates muscle point; AC, acromion; OL, olecranon.
0.965 0.713 0.126 0.012 0.093 0.211 j0.001 0.01 0.05 j0.04 j0.02 j0.02 0.374 0.457 0.746 0.001 0.003 0.008 j0.02 j0.02 0.01 j0.05 j0.04 j0.05 0.975 0.589 0.955 0.028 0.060 0.013 j0.001 0.01 0.002 j0.03 j0.03 j0.04 0.278 0.594 0.274 0.003 0.008 0.182 j0.03 j0.01 0.04 j0.04 j0.04 j0.02 0.560 0.776 0.709 0.002 0.018 0.052 j0.01 j0.01 0.01 j0.04 j0.029 j0.03 0.571 0.451 0.828 0.363 0.981 0.351 j0.01 j0.02 0.01 j0.01 0.000 j0.02 0.531 0.464 0.813 0.135 0.324 0.235 j0.01 j0.02 0.01 j0.02 j0.01 j0.02 0.286 0.321 0.190 0.119 0.450 0.090 j0.02 j0.02 j0.04 j0.02 j0.01 j0.02 0.224 0.244 0.576 0.116 0.224 0.568 j0.03 j0.03 0.02 j0.02 j0.02 j0.01 0.132 0.118 0.819 0.016 0.066 0.527
P B P B P B P B P B P B P B P B P B
j0.03 j0.03 j0.01 j0.03 j0.02 j0.01 MP1b MP2c MP3d MP1a MP2c MP3d Healthy side VRS at VRS at VRS at Hemiparetic VRS at VRS at side VRS at
Pa Ba
PPT at OL
a a
PPT at AC
a
PPT at MP3
a a
PPT at MP2
a a a a
PPT at AC
a a
PPT at MP3
a a
PPT at MP2
a a
PPT at MP1
a
PPT at OL
a
PPT at MP1
a
Hemiparetic Side Healthy Side TABLE 6 Association between spontaneous pain and PPT
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between ipsilateral MTePs and periostea (relative PPTs) were also analyzed to eliminate the influence of hemiparetic-side sensory deficit. However, both the absolute PPTs and the relative PPTs were not significantly different between the hemiparetic side and the healthy side, even in the subjects with moderate to severe spontaneous pain in the hemiparetic side. One unexpected finding was that there was a trend toward slightly decreased sensitivity to pressure pain in the brachioradialis muscle in the hemiparetic side. Nevertheless, this might be caused by post-stroke sensory deficit, which could involve the distal limb more than the proximal shoulder girdle. The PPT was lowest (most sensitive to pressure pain) during the first 3 mos of stroke duration in both the hemiparetic and healthy sides and successively increased as the stroke duration increased, although the difference between stroke duration of 3 mos to 1 yr and more than 1 yr was modest. Although PPT levels before stroke were not known and there was no healthy control group for comparison, the PPT values at the upper trapezius region in the present study were apparently lower than those reported from one recent PPT topography study in healthy young adults.17 Thus, the PPT was assumed to become lower after stroke and gradually returned to baseline along with the course of the stroke, which indicated the existence of post-stroke sensitization. This sensitization phenomenon leading to increased sensitivity to pressure pain was correlated with the VRS score in the hemiparetic side and was not limited to the MTeP with spontaneous pain itself and also spread to other muscles and periosteum points bilaterally, disregarding the hemiparetic-side involvement of the stroke (Table 6). The Bspreading[ of the sensitization was more diffusely triggered by the upper trapezius MTePs, possibly because of the higher spontaneous pain intensity that occurred in the upper trapezius than in the brachioradialis (Table 6). This phenomenon might be related to a so-called central or extrasegmental sensitization mechanism; it has also been found in other pain disorders such as carpal tunnel syndrome and shoulder impingement syndrome.12,13 For example, one may have pain syndrome in the shoulder, whereas the PPT level could also be reduced in the lower leg muscle.13 This might explain why central post-stroke pain or other pain syndromes could also involve the healthy side of stroke patients4,10 and partly explain why the subjects had higher spontaneous pain intensity in the hemiparetic side but had symmetric PPT in both sides in the present study. The sensitized pressure pain hyperalgesia might be secondary to nociceptive Muscle Pain in Patients With Stroke
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input from post-stroke hemiparetic pain, but other mechanisms such as brain damage from the stroke itself or an abnormality in muscle balance could also be contributive.
Sex and Age Influences on Pain Perception This study found that the female sex was more sensitive to pressure pain stimulation and was associated with higher VRS scores in the MTePs of the hemiparetic side during the first few months after stroke. These findings were consistent with current evidences that women have lower PPTs than men do18 and are more likely to have chronic pain syndrome or more severe pain intensity in both the stroke population and the general population.4,19 The associations between age and pain perception are inconsistent in previous studies.20 One study of pain prevalence of stroke reported that pain intensity was lower in older stroke patients.4 However, another study revealed no association between age and shoulder pain on the hemiparetic side.7 Age effect on pain perception varies from different pain stimuli. It is reported that older subjects are more sensitive to pressure pain but are less sensitive to heat pain, and there are no age-related changes from electrical-currentYinduced pain.20Y22 In this study, age was not associated with spontaneous muscle pain but was negatively correlated with PPT when analyzed by univariate analysis (Table 3), which indicates that older stroke patients are more sensitive to pressure pain, although it lost the statistical significance when analyzed by multivariate linear regression. This could possibly be explained by the fact that the age difference in the present study was not as distinct as in the study of Lautenbacher et al.,21 which enrolled 20 young subjects between the ages of 21 and 35 yrs (mean T SD age, 27.1 T 3.5 yrs) and 20 older subjects between the ages of 63 and 88 yrs (mean age, 71.6 T 5.9 yrs).
Characteristics of Spontaneous Pain and PPT Topography This study found that VRS scores and PPTs were significantly different among different MTePs. However, the rank orders of VRS scores and PPTs among each MTeP were different (VRS scores in decreasing order: MTeP 2, MTeP 1, and MTeP 3 vs. sensitivity to pressure pain in decreasing order: MTeP 1, MTeP 3, and MTeP 2). The finding of higher VRS scores noted in the upper trapezius than scores in the brachioradialis muscle was expected because the former would be more affected
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by nearby hemiparetic shoulder pain, a frequent problem in stroke patients.4,7,9 Furthermore, the PPTs were symmetric bilaterally, which was in agreement with a recent topographic study of PPT12,17 that revealed the characteristic distribution of PPTs. Meanwhile, the present study found that this symmetrically distributed topography seemed not to be changed by the existence of hemiparesis or hemiplegia through the central or the extrasegmental sensitization process mentioned above. However, a further study with a large sample size is needed for confirmation.
Limitations of This Study The present study has several limitations. Firstly, VRS or PPT data from the subjects before stroke were not available for comparison in this cross-sectional study. Despite obvious increased intensity of spontaneous muscle pain in the hemiparetic side than in the healthy side, the exact extent of intensity change after stroke or whether the pain existed before stroke could not be known. Similarly, PPT levels before stroke were not known, and there was also no healthy control group for comparison. The assumption for post-stroke sensitization was made from comparisons of the PPT values with those reported from the previous study.17 Secondly, patients with serious illness or cognitive deficit such as impaired consciousness and aphasia, which could cause difficulty in evaluation of the VRS or PPT, were excluded from this study. On the other hand, patients with minor dysfunction from stroke might not go to a rehabilitation center and would not be included in this study. This may result in selection bias with inclusion of patients with a smaller range of severity of stroke. Thus, the results could not be representative for all stroke patients. This might cause difficulty in determining the association between pain symptoms and motor deficit measured with muscle power or the Brunnstrom stage, as reported in a previous study that showed that hemiparetic-side shoulder pain was associated with the degree of arm weakness.7 Thirdly, because of the cross-sectional design of this study, the data of VRS or PPT for analysis were from each patient with different durations of stroke but not from the same patient in different temporal courses. The results were generalized by adjusting the possible confounding factors among each individual such as age and sex but not from longitudinal observation. Finally, no information was available about whether any analgesic or muscle relaxant drugs
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were given at the time of investigation, and data were lacking regarding location, size, or degree of the cerebrovascular event. A further study would be needed to include this information.
CONCLUSIONS Stroke patients have the highest spontaneous muscle pain intensity and are most sensitive to pressure pain within 3 mos of stroke. Spontaneous muscle pain is more severe in the hemiparetic side than in the healthy side, but no differences are seen in the PPT of the muscle or the periosteum between the two sides. Bilateral symmetric lowering of PPT associated with hemiparetic-side spontaneous muscle pain intensity is assumed to be caused by central sensitization. Further investigation is needed to clarify the underlying mechanism.
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