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Effect of acupuncture treatment on spastic states of stroke patients
Journal of the Neurological Sciences 276 (2009) 143–147
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Effect of acupuncture treatment on spastic states of stroke patients Jian-Guo Zhao, Chen-Hong Cao, Cun-Zhi Liu ⁎, Bao-Jie Han, Jie Zhang, Zu-Guang Li, Tao Yu, Xu-Hui Wang, Hong Zhao, Zhen-Hua Xu The First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, 314 Anshanxi Road, Tianjin, 300193, China
a r t i c l e
i n f o
Article history: Received 22 April 2008 Received in revised form 15 September 2008 Accepted 16 September 2008 Available online 30 October 2008 Keywords: Acupuncture Spasticity Stroke Muscle tone Motor neuron excitability
a b s t r a c t Purposes: The control of spasticity is often a significant problem in the management of patients with stroke. The aim of this study was to evaluate the effect of acupuncture treatment on the spastic states of stroke patients. Setting: An outpatient Acupuncture Department in the First Teaching Hospital of Tianjin University of Traditional Chinese Medicine. Participants: One hundred and thirty-one patients, mean (SD) age of 59 (12) years, with spastic hemiplegia were included at mean (SD) month of 17 (7) months after stroke. Intervention: Participants received two 30-day treatment regimens: combined stimulating surface projection zone of decussation of pyramid and traditional acupuncture treatment, and traditional acupuncture treatment only. Main outcome measures: Differences in the modified Ashworth scale (MAS), Fugl–Meyer Assessment (FMA), Barthel Index (BI), and the electromyographic activity of the affected extremity between arms. Results: The average (±SD) upper extremity Ashworth score significantly decreased, from 3.08± 0.77 before treatment to 1.82 ± 0.65 after acupuncture intervention (wrist joint, P b 0.05), and from 2.72 ± 0.59 to 1.32 ± 0.71 (elbow joint, P b 0.05) for treatment group. There were significant differences noted between the treatment group and control group after administration. Lower extremity treatment responses were similar to upper extremity responses. However, both groups showed similar improvement in FMA (upper extremity) and FMA (lower extremity). However, the improvements of FMA (total), BI, and F/M ratio were better in treatment group than in control group. Conclusions: These results suggested that acupuncturing surface projection zone of decussation of pyramid was effective in reducing spastically increased muscle tone and motor neuron excitability in spastic hemiplegia, and could improve spastic states of stroke patients, thus providing a safe and economical method for treating stroke patients. © 2008 Elsevier B.V. All rights reserved.
1. Introduction After recovery from a stroke, a patient can frequently have motor weakness on one or both sides of the body. Further impairing mobility and function in this patient population is spastic hypertonia. This excessive muscle tone can cause many problems, including pain, loss of free movement of a limb, and interference with the ability to walk and perform daily activities, such as bathing or dressing [1]. It also may cause the limb to become “fixed” or frozen in an uncomfortable position. The pharmaceutical management of spastic hypertonia following stroke has generally been confined to the use of approaches that diminish peripheral cholinergic activity at the neuromuscular junction (botulinum toxin), inhibit the release of calcium from the sarcoplasmic reticulum (dantrolene sodium), or those that act centrally [2–5]. In this latter class, there are 3 primary medications: ⁎ Corresponding author. Tel.: +86 22 27432208; fax: +86 22 27432227. E-mail address: [email protected] (C.-Z. Liu). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.09.018
baclofen, diazepam, and clonidine. These procedures generally require repetition and have been associated with permanent weakness, dysesthesias, and causalgia [6]. Acupuncture is one of the main modalities of treatment in traditional Chinese medicine (TCM) and can be traced back more than 2000years in China. It was widely used to treat hemiplegia long before the Tang dynasty. There are numerous reports that acupuncture could improve post stroke motor ability [7,8]. However, the efficacy of acupuncture was rarely reported in spastic hypertonia from stroke. This report describes a prospective, single-blinded study of acupuncture treatment in stroke patients with spastic hypertonia. 2. Methods 2.1. Subjects In this study, 131 patients in total with spastic hypertonia from stroke were chosen from October 2003 through June 2005. After the
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initial screening evaluation, patients were enrolled in the study if they met all of the following criteria: (1) Chinese patients with hemorrhagic or ischemic stroke (either CT scan confirmed or CT scan normal but clinically consistent with the World Health Organization's definition of stroke), (2) diagnosis of spastic hypertonia in extremities that was defined by an average Ashworth score of at least 1 in one affected extremity at the day of the first screening, and (3) the duration of the disease should be 2weeks at least. A complete physical examination and neurological assessment and a thorough history of spasticity were assessed before the trial was performed.
between the baseline and final scores within each arm. The physician examining the patients and carrying out the measurements was unaware of what kind of treatment each subject received. The measurements were made by the same investigator in a temperature-controlled room. 2.4.1. Modified Ashworth Scale (MAS) The modified Ashworth scale (range, 0–4) [12–14] was used to assess muscle tone in both the lower extremities (hip abduction, hip flexion, knee flexion, and ankle dorsiflexion) and the upper extremities (shoulder abduction, elbow extension, elbow flexion, and wrist extension).
2.2. Design and setting The study was a prospective, single-blinded, randomized clinical trial carried out in Acupuncture Department in the First Teaching Hospital of Tianjin University of Traditional Chinese Medicine. Each patient signed an informed consent form prior to testing. 2.3. Acupuncture treatment Patients were randomized before the treatment to either treatment group (TG) or control group (CG) by means of a random number table. Both the TG and the CG received routine treatment as other outpatients with stroke, including routine pharmacologic and traditional acupuncture treatment. Routine medications for stroke included antiplatelet agents and anticoagulants, antihypertensive, hypoglycemic and antihyperlipidemic drugs. These medicines should be taken following the advice of physician and according to symptoms of each patient. The CG received traditional acupuncture treatment. The prescription comprising Neiguan (PC6), Sanyinjiao (SP6), Shuigou (GV26), Jiquan (HT1), Chize (LU5) Weizhong (BL40) and Fengchi (GB20) has been proved to be effective in curing patients with cerebrovascular lesion and subsequent disabled state [9–11]. Selection of the 7 main acupoints was based on the TCM theory. Sterile acupuncture needles (Huatuo, Suzhou Medical Instruments Factory, Suzhou, China), with a diameter of 0.25–0.30mm, were used in the trial. Once a characteristic aching and tingling sensation (known as “DeQi” meaning “obtained essence”) was elicited, the needle would be removed. Apart from traditional acupuncture treatment, the TG received the stimulation of surface projection zone of decussation of pyramid, which located at the junction between Yuzhen (BL9) and Tianzhu (BL10), and four equidistant points were chosen. Needles were inserted horizontally 15mm. After getting the needle sensation, the needle would be kept in situ for 20min. Treatment in the two groups should be performed once daily for 30days. Adverse reactions that occurred during acupuncture sessions were reported to the principal investigator, who would decide whether the trial should be terminated. Patients who had defaulted for 3 times would be treated as having dropped out of the trial. Causes of death and other reasons for withdrawal were also recorded. 2.4. Measurements Baseline characteristics and co morbidity of the enrolled patients, impairments and complications were all recorded. The outcome measures were assessed at baseline and after the intervention (within 3days after acupunctural treatment). Our test battery consisted of four measurements including the modified Ashworth scale (MAS), Fugl–Meyer Assessment (FMA), Barthel Index (BI), and the electromyographic activity of the affected extremity. Main outcome measure was the difference in MAS, FMA, BI, and EMG between arms. Predefined secondary outcome was the comparisons
2.4.2. Fugl–Meyer assessment (FMA) of motor performance FMA is a well-validated instrument assessing motor recovery after stroke, and has been widely used for both clinical and research purposes [15,16]. 2.4.3. Barthel index (BI) BI is a validated and widely used instrument to measure disability in ADL [17,18]. It has a total BI score of 100. The severity of disability is classified as mild (BI z 75), moderate to severe (20 b BI b 75), and very severe (BI V 20). 2.4.4. Electromyography (EMG) The electromyography system (Keypoint, DADTEC Biomedical Inc., Denmark) was used to perform nerve stimulation and reflex recording, before and after the 30-day treatment. The skin resistance overlying the abductor hallucis and extensor digitorum muscle were made as minimal as possible by shaving the area and brushing it with alcohol. The muscle responses were recorded through two silverchloride EMG electrodes, 9mm in diameter, coated with conducting cream. F-waves were evoked using a rectangular voltage pulse, 0.5ms in duration, by the stimulator. The stimulator was placed over the distal to the peroneal nerve and median nerve. The F-wave parameters were recorded and the F/M ratio was calculated by dividing the mean value of 10 F-waves by the mean value of 3Mresponses. 2.5. Statistical analysis For this pilot study, recruitment was limited by administrative factors. Therefore, it was projected that 120 eligible participants could be recruited and treated. The results were presented as mean ± SD. χ2 test, t-test and Wilcoxon test were used to compare the demographic characteristics and other variables of the 2 groups where appropriate. A value of P b 0.05 was considered significant. Statistical analysis was performed with SPSS version 10.0 (SPSS Inc., Chicago, Illinois, USA). 3. Results A total of 131 Chinese patients were enrolled and randomized to treatment group (n = 67) and control group (n = 64) in the present study. Patient baseline characteristics were comparable between the two groups (Table 1). No significant differences were found between the two groups for age, gender, stroke type, or time from stroke onset to be randomized (all Ps N 0.05). Among all the patients, no adverse effects were caused by the acupuncture treatment. Eleven patients dropped out during the trial, accounting for a 9% dropout rate. There were no deaths or protocol violators during the trial. Among the 11 dropouts, 3 patients had recurrent stroke; 6 defaulted on treatments; and 2 patients withdrew because they could not be discharged within the defined period because of a social problem. There was no statistical difference in dropouts between the 2 groups (Fig. 1).
J.-G. Zhao et al. / Journal of the Neurological Sciences 276 (2009) 143–147 Table 1 Baseline characteristics of the spastic hypertonia patients Characteristics
Treatment group (n = 67) Control group (n=64)
Age, y (mean ± SD) Gender Male Female Duration(since stroke), m (mean± SD) Stroke type Infarct Hemorrhage
58.50 ± 11.60
60.27 ± 11.71
52 15 16.34 ± 6.09
48 16 16.76 ± 6.89
49 18
51 13
Table 2 summarizes the MAS, FMA and BI baseline, post-treatment and change scores for stroke patients with spastic states. A modified Ashworth scale was used to evaluate the muscle tone of the main joints. Overall, the average (±SD) upper extremity Ashworth score significantly decreased, from 3.08 ± 0.77 at baseline to 1.82 ± 0.65 after acupuncture intervention (wrist joint, P b 0.05), and from 2.72 ± 0.59 baseline to 1.32 ± 0.71 after acupuncture intervention (elbow joint, P b 0.05). No significant baseline difference was observed in average upper extremity Ashworth score between treatment group and control group (P N 0.05). However, there were significant differences noted between the treatment group and control group after administration (P b 0.05). Lower extremity treatment responses were similar to upper extremity responses. The average (±SD) lower extremity Ashworth score significantly decreased, from 2.30 ± 0.59 at baseline to
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1.15 ± 0.48 after treatment (knee joint, P b 0.05), and from 3.02 ±0.68 at baseline to 1.67 ± 0.71 after treatment (ankle joint, P b 0.05). No significant baseline difference was observed in average lower extremity Ashworth score between treatment group and control group (P N 0.05). However, there were significant differences noted between the treatment group and control group after administration (P b 0.05). Furthermore, examination of the changes in MAS scores after treatment revealed that compared to the control group the improvement was significantly greater in the treatment group (all Ps b 0.05). At baseline, no differences between the two groups were found for the FMA or BI score. We found that there were significant differences between pre-treatment and post-treatment for the scores of FMA (upper extremity), FMA (lower extremity), FMA (total) and BI (P b 0.05, for all) in both treatment group and control group. In fact, both groups showed similar improvement in FMA (upper extremity) and FMA (lower extremity). Only the improvements of FMA (total) and BI were better in treatment group than in control group. However, as with the functional improvement analysis, there were statistically significant differences between the control and treatment groups when comparing the change scores for both the total and subscale FMA (P b 0.05, for all) (Table 2). In addition, Table 2 summarizes the EMG baseline and posttreatment activities for spastic patients. The F/M ratios of upper extremity of the two groups between pre-treatment and posttreatment were significantly different (P b 0.05). The F/M ratio of lower extremity also decreased significantly as compared to the pre-
Fig. 1. Trial flow diagram.
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Table 2 Outcome changes between the two groups Outcome measure muscle tone (wrist joint) muscle tone (elbow joint) muscle tone (knee joint) muscle tone (ankle joint) FMA (upper extremity) FMA(lower extremity) FMA (total) BI EMG (upper extremity) F-wave amplitude (mean) F-wave amplitude (max) F/M ratio EMG(lower extremity) F-wave amplitude (mean) F-wave amplitude (max) F/M ratio
Treatment group
Control group
Baseline
After treatment
Change
Baseline
After treatment
Change
3.08 ± 0.77 2.72 ± 0.59 2.30 ± 0.59 3.02 ± 0.68 34.12 ± 3.96 17.63 ± 1.68 51.75 ± 4.97 41.83 ± 8.88
1.82 ± 0.65*△ 1.32 ± 0.71*△ 1.15 ± 0.48*△ 1.67 ± 0.71*△ 42.80 ± 3.74* 22.90 ± 1.98* 65.70 ± 4.91*△ 65.25 ± 8.95*△
1.27 ± 0.69△ 1.40 ± 0.59△ 1.15 ± 0.55△ 1.35 ± 0.58△ 8.73 ± 2.19△ 5.35 ± 2.21△ 14.08 ± 3.73△ 23.92 ± 5.76△
2.92 ± 0.70 2.52 ± 0.64 2.12 ± 0.64 3.02 ± 0.65 34.67 ± 3.08 17.75 ± 1.74 52.42 ± 3.72 39.83 ± 8.13
2.65 ± 0.93* 1.90 ± 0.78* 1.70 ± 0.81* 2.93 ± 0.86 41.68 ± 3.44* 22.22 ± 1.68* 63.90 ± 4.55* 59.92 ± 8.16*
0.27 ± 0.48 0.68 ± 0.57 0.45 ± 0.50 0.15 ± 0.51 7.02 ± 1.91 4.47 ± 1.36 11.48 ± 2.94 20.25 ± 5.71
0.37 ± 0.14 0.54 ± 0.36 0.10 ± 0.07
0.25 ± 0.08*△ 0.33 ± 0.13*△ 0.05 ± 0.04*△
0.40 ± 0.24 0.56 ± 0.22 0.12 ± 0.08
0.34 ± 0.19* 0.57 ± 0.29 0.09 ± 0.06*
0.29 ± 0.17 0.55 ± 0.27 0.12 ± 0.11
0.17 ± 0.07*△ 0.35 ± 0.21*△ 0.05 ± 0.03*△
0.33 ± 0.16 0.65 ± 0.27 0.14 ± 0.07
0.31 ± 0.15 0.52 ± 0.20* 0.10 ± 0.05*
*p b 0.05, compared with pre-treatment; △p b 0.05, compared with control group.
treatment ratio (P b 0.05). However, the improvements of the F/M ratios were better in treatment group than in control group. 4. Discussion Spasticity has been defined as a motor disorder characterized by a velocity-dependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as a component of the upper motoneuron syndrome [19,20]. The increased muscle tone may be noted in all affected synergistic muscle groups following a stroke, thereby reducing functional motor activities. Although there are numerous approaches to the treatment of spasticity, many patients are still unable to find a satisfactory method of managing their spasms with acceptable side effects. In the present study, the effectiveness of acupuncture on spasticity was evaluated by independent, blinded assessors for tone, motor performance, daily activities and electromyography. Our results have shown significant improvement in muscle tone, motor impairment, and disability in patients receiving combined acupuncture treatment as compared with the control. Some previous studies [21,22] have also shown the effect of acupuncture treatment on the reduction in spasticity using clinical measurements. The clinical measurement using MAS scores showed a similar reduction like the quantitative measurement in our study. Acupuncture may change the motoneuron activity and/or change synaptic transmission from muscle afferent terminals to spinal motoneurons, presumably mediated by presynaptic interneurons, and change intrinsic motoneuron properties, including membrane input resistance or membrane receptor responsiveness to released transmitters [23]. A recent study showed that acupuncture led to immediate and short-term plastic brain reorganization in comparison to needling at non-acupuncture points in healthy subjects [24]. Hence, acupuncture treatment for stroke motor impairment can be more efficacious than traditional approaches, which focus on impairment. The importance of sensory stimulation in stimulating the brain and facilitating recovery has been shown with functional MRI and is likely the physiological underpinning for the use of acupuncture for facilitating motor recovery. Acupuncture has also been shown to suppress the amplitude of somatosensory evoked potentials in both humans and animals [25]. The junction between Yuzhen (BL9) and Tianzhu (BL10) in Bladder meridian of foot-taiyang is the surface projection zone of decussation of pyramid, and is spatially correlated with the areas of the motor tracts controlling liberomotor function of specific parts of the body, although the cranial bone separates them and the focus lies in the deeper portion of the brain. Stimulating the acupoints along these
meridians can facilitate the restoration of motor impairment and disability. Furthermore, there have been classical acupuncture treatments in the body acupoints (including the head) for strokes, which mainly adopted activating brain and regaining consciousness needling method, which has been proved to be effective in improving a disabled state [9–11]. These suggest that there are at least two pathways, for example afferent and efferent connecting with the damaged parts of the brain. This appears to show some parallelism with rehabilitation therapy involving stimulation and motivation [26]. It is likely that acupuncture is much more direct and effective. The characteristics of spasticity could be related to changes in neurophysiology and muscle properties. The alterations in F-wave parameters in spasticity are more precise for assessment of alpha motoneuron excitability than the well known T and H-reflexes [27– 29]. In the present study, we used the F/M ratio to measure changes in motor neuron excitability, which made changes in the mechanism of spasticity clearer from the neurological standpoint. We found that the F-wave in amplitude (mean and maximal) and the F/M ratios significantly decreased after acupuncturing surface projection zone of decussation of pyramid (p b 0.05). This result indicated that the acupuncture treatment could inhibit the neuron excitability in patients with spastic hypertonia from stroke. A few comments about our method of design and our study limitations deserve mention. First, one potential limitation of the study is that as a pilot study, no power analysis was provided in this study, which lowered the statistical power of the study to a certain extent. Second, another limitation is that many variables were assessed in the present study and did not have a primary outcome measure. Combined clinical and neurophysiologic evaluation of acupuncture response among stroke patients with spastic states has not been previously described. Thus, our primary objective was to evaluate changes in the Ashworth Scale, Fugl–Meyer Assessment, Barthel Index, and EMG activity after acupuncture treatment for spastic hypertonia resulting from stroke. Third, although the study evaluators were blinded to the treatment assignment, the patients were not blinded. Therefore, one of the limitations of this pilot study is that we did not measure the effect of patient expectation. Furthermore, the follow-up data after treatment were not available. Although the initial study plan considered a long-term follow-up, limited resources did not permit patient post-treatment clinic or home visits for assessing spastic states and motor function. Finally, no sham acupuncture was used in this pilot study. Therefore there was no guarantee that the placebo effect of the acupuncture treatment had been removed completely from the results, even though taking the routine treatment group as control in the present study.
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In conclusion, there was a significant reduction in spasticity after a 30-day acupuncture treatment, and this improvement was likely related with reduced excitability of alpha-motoneurons. Further work is needed to establish the possible mechanism responsible for the acupuncture treatment inducing inhibitory effects on alphamotoneurons. Acknowledgment This study was supported by the Bureau of Public Health of Tianjin (Nos. 03046 and 07059), and the promotion project of the ministry of health of the people's republic of China (No. Weitong [2007]13). References [1] Meythaler JM, McCary A, Hadley MN. Intrathecal baclofen for spastic hypertonia in adult brain injury. Perspect Neurosurg 1996;7:99–107. [2] Saulino M, Jacobs BW. The pharmacological management of spasticity. J Neurosci Nurs 2006;38(6):456–9. [3] Hesse S, Werner C. Poststroke motor dysfunction and spasticity: novel pharmacological and physical treatment strategies. CNS Drugs 2003;17(15):1093–107. [4] Meythaler JM, Guin-Renfroe S, Johnson A, Brunner RM. Prospective assessment of tizanidine for spasticity due to acquired brain injury. Arch Phys Med Rehabil 2001;82(9):1155–63. [5] Meythaler JM, Guin-Renfro S, Law C, Grabbe PA, Hadley MN. Continuously infused intrathecal baclofen (ITB) for spasticity/dystonia in older children, adolescents and adults with cerebral palsy. Arch Phys Med Rehabil 2000;82:155–61. [6] Ford B, Green P, Louis ED, Petzinger G, Bressman SB, Goodman R, et al. Use of intrathecal baclofen in the treatment of patients with dystonia. Arch Neurol 1996;53:1241–6. [7] Wong AMK, Su TY, Tang FT, Cheng PT, Liaw MY. Clinical trial of electrical acupuncture on hemiplegic stroke patients. Am J Phys Med Rehabil 1999;78:117–22. [8] Sallstrom S, Kjendahl A, Osten PE, Stanghelle JH, Borchgrevink CF. Acupuncture in the treatment of stroke patients in the subacute stage: a randomized, controlled study. Complementary Ther Med 1996;4:193–7. [9] Shi X, Yang Z, Zhang C, Zhou J, Han J, Wu L, et al. Clinical observations on acupuncture treatment of pseudobulbar palsy—a report of 325 cases. J Tradit Chin Med 1999;19(1):27–31. [10] Bian JL, Zhang CH, Li JB, Zhang Y, Ding SQ, He J, et al. Observation on therapeutic effect of activating brain function to cause resuscitation needling method on deglutition disorders after stroke. Zhongguo Zhen Jiu 2005;25(5):307–8. [11] Shen PF, Kong L, Shi XM. Study on clinical therapeutic effect of activating brain and regaining consciousness needling method on poststroke depression and the mechanism. Zhongguo Zhen Jiu 2005;25(1):11–3.
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[12] Meythaler JM, McCary A, Hadley MN. Prospective study on the use of continuously infused intrathecal baclofen for spasticity due to acquired brain injury: a preliminary report. J Neurosurg 1997;87:415–9. [13] Meythaler JM, Renfroe SG, Grabb PA, Hadley MN. Long-term continuously infused intrathecal baclofen for spastic/dystonic hypertonia in traumatic brain injury: 1-year experience. Arch Phys Med Rehabil 1999;80:13–9. [14] Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987;67(2):206–7. [15] Albright LA, Barron WB, Fasick MP, Polinko P, Janosky J. Continuous intrathecal baclofen infusion for spasticity of cerebral origin. JAMA 1993;270:2475–7. [16] Knuttson E, Lindblom U, Martensson A. Plasma and cerebrospinal fluid levels of baclofen (Lioresal) at optimal therapeutic responses in spastic paresis. J Neurol Sci 1974;23:473–84. [17] Grabb PA, Guin-Renfroe S, Meythaler JM. Midthoracic catheter tip placement for intrathecal baclofen administration in children with quadriparetic spasticity. Neurosurgery 1999;45:833–7. [18] Meythaler JM, DeVivo MJ, Hadley MN. Prospective study on the use of bolus intrathecal baclofen for spastic hypertonia due to acquired brain injury. Arch Phys Med Rehabil 1996;77:461–6. [19] Lance J. Symposium synopsis. In: Feldman R, Young R, Koella W, editors. Spasticity: disordered motor control. Chicago: Year Book Medical Publishers; 1980. p. 485–94. [20] Lamontagne A, Malouin F, Richards CL, Dumas F. Evaluation of reflex- and nonreflex-induced muscle resistance to stretch in adults with spinal cord injury using hand-held and isokinetic dynamometry. Phys Ther 1998;78(9):964–75 discussion 976–8. [21] Mukherjee M, McPeak LK, Redford JB, Sun C, Liu W. The effect of electroacupuncture on spasticity of the wrist joint in chronic stroke survivors. Arch Phys Med Rehabil 2007;88(2):159–66. [22] Wong AM, Su TY, Tang FT, Cheng PT, Liaw MY. Clinical trial of electrical acupuncture on hemiplegic stroke patients. Am J Phys Med Rehabil 1999;78:117–22. [23] Lee JH, Beitz AJ. Electroacupuncture modifies the expression of c-fos in the spinal cord induced by noxious stimulation. Brain Res 1992;577:80–91. [24] Lo YL, Cui SL, Fook-Chong S. The effect of acupuncture on motor cortex excitability and plasticity. Neurosci Lett 2005;384:145–9. [25] Meissner W, Weiss T, Trippe RH, Hecht H, Krapp C, Miltner WH. Acupuncture decreases somatosensory evoked potential amplitudes to noxious stimuli in anesthetized volunteers. Anesth Analg 2004;98:141–7. [26] Inoue I, Chen L, Zhou L, Zeng X, Wang H. Reproduction of scalp acupuncture therapy on strokes in the model rats, spontaneous hypertensive rats-stroke prone (SHR-SP). Neurosci Lett 2003;333(3):191–4. [27] Milanov IG. F-wave for assessment of segmental motoneurone excitability. Electromyogr Clin Neurophysiol 1992;32(1–2):11–5. [28] Dressnandt J, Auer C, Conrad B. Influence of baclofen upon the alpha-motoneuron in spasticity by means of F-wave analysis. Muscle Nerve 1995;18(1):103–7. [29] Milanov I, Georgiev D. Mechanisms of tizanidine action on spasticity. Acta Neurol Scand 1994;89(4):274–9.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j n s
Effect of acupuncture treatment on spastic states of stroke patients Jian-Guo Zhao, Chen-Hong Cao, Cun-Zhi Liu ⁎, Bao-Jie Han, Jie Zhang, Zu-Guang Li, Tao Yu, Xu-Hui Wang, Hong Zhao, Zhen-Hua Xu The First Teaching Hospital of Tianjin University of Traditional Chinese Medicine, 314 Anshanxi Road, Tianjin, 300193, China
a r t i c l e
i n f o
Article history: Received 22 April 2008 Received in revised form 15 September 2008 Accepted 16 September 2008 Available online 30 October 2008 Keywords: Acupuncture Spasticity Stroke Muscle tone Motor neuron excitability
a b s t r a c t Purposes: The control of spasticity is often a significant problem in the management of patients with stroke. The aim of this study was to evaluate the effect of acupuncture treatment on the spastic states of stroke patients. Setting: An outpatient Acupuncture Department in the First Teaching Hospital of Tianjin University of Traditional Chinese Medicine. Participants: One hundred and thirty-one patients, mean (SD) age of 59 (12) years, with spastic hemiplegia were included at mean (SD) month of 17 (7) months after stroke. Intervention: Participants received two 30-day treatment regimens: combined stimulating surface projection zone of decussation of pyramid and traditional acupuncture treatment, and traditional acupuncture treatment only. Main outcome measures: Differences in the modified Ashworth scale (MAS), Fugl–Meyer Assessment (FMA), Barthel Index (BI), and the electromyographic activity of the affected extremity between arms. Results: The average (±SD) upper extremity Ashworth score significantly decreased, from 3.08± 0.77 before treatment to 1.82 ± 0.65 after acupuncture intervention (wrist joint, P b 0.05), and from 2.72 ± 0.59 to 1.32 ± 0.71 (elbow joint, P b 0.05) for treatment group. There were significant differences noted between the treatment group and control group after administration. Lower extremity treatment responses were similar to upper extremity responses. However, both groups showed similar improvement in FMA (upper extremity) and FMA (lower extremity). However, the improvements of FMA (total), BI, and F/M ratio were better in treatment group than in control group. Conclusions: These results suggested that acupuncturing surface projection zone of decussation of pyramid was effective in reducing spastically increased muscle tone and motor neuron excitability in spastic hemiplegia, and could improve spastic states of stroke patients, thus providing a safe and economical method for treating stroke patients. © 2008 Elsevier B.V. All rights reserved.
1. Introduction After recovery from a stroke, a patient can frequently have motor weakness on one or both sides of the body. Further impairing mobility and function in this patient population is spastic hypertonia. This excessive muscle tone can cause many problems, including pain, loss of free movement of a limb, and interference with the ability to walk and perform daily activities, such as bathing or dressing [1]. It also may cause the limb to become “fixed” or frozen in an uncomfortable position. The pharmaceutical management of spastic hypertonia following stroke has generally been confined to the use of approaches that diminish peripheral cholinergic activity at the neuromuscular junction (botulinum toxin), inhibit the release of calcium from the sarcoplasmic reticulum (dantrolene sodium), or those that act centrally [2–5]. In this latter class, there are 3 primary medications: ⁎ Corresponding author. Tel.: +86 22 27432208; fax: +86 22 27432227. E-mail address: [email protected] (C.-Z. Liu). 0022-510X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.jns.2008.09.018
baclofen, diazepam, and clonidine. These procedures generally require repetition and have been associated with permanent weakness, dysesthesias, and causalgia [6]. Acupuncture is one of the main modalities of treatment in traditional Chinese medicine (TCM) and can be traced back more than 2000years in China. It was widely used to treat hemiplegia long before the Tang dynasty. There are numerous reports that acupuncture could improve post stroke motor ability [7,8]. However, the efficacy of acupuncture was rarely reported in spastic hypertonia from stroke. This report describes a prospective, single-blinded study of acupuncture treatment in stroke patients with spastic hypertonia. 2. Methods 2.1. Subjects In this study, 131 patients in total with spastic hypertonia from stroke were chosen from October 2003 through June 2005. After the
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initial screening evaluation, patients were enrolled in the study if they met all of the following criteria: (1) Chinese patients with hemorrhagic or ischemic stroke (either CT scan confirmed or CT scan normal but clinically consistent with the World Health Organization's definition of stroke), (2) diagnosis of spastic hypertonia in extremities that was defined by an average Ashworth score of at least 1 in one affected extremity at the day of the first screening, and (3) the duration of the disease should be 2weeks at least. A complete physical examination and neurological assessment and a thorough history of spasticity were assessed before the trial was performed.
between the baseline and final scores within each arm. The physician examining the patients and carrying out the measurements was unaware of what kind of treatment each subject received. The measurements were made by the same investigator in a temperature-controlled room. 2.4.1. Modified Ashworth Scale (MAS) The modified Ashworth scale (range, 0–4) [12–14] was used to assess muscle tone in both the lower extremities (hip abduction, hip flexion, knee flexion, and ankle dorsiflexion) and the upper extremities (shoulder abduction, elbow extension, elbow flexion, and wrist extension).
2.2. Design and setting The study was a prospective, single-blinded, randomized clinical trial carried out in Acupuncture Department in the First Teaching Hospital of Tianjin University of Traditional Chinese Medicine. Each patient signed an informed consent form prior to testing. 2.3. Acupuncture treatment Patients were randomized before the treatment to either treatment group (TG) or control group (CG) by means of a random number table. Both the TG and the CG received routine treatment as other outpatients with stroke, including routine pharmacologic and traditional acupuncture treatment. Routine medications for stroke included antiplatelet agents and anticoagulants, antihypertensive, hypoglycemic and antihyperlipidemic drugs. These medicines should be taken following the advice of physician and according to symptoms of each patient. The CG received traditional acupuncture treatment. The prescription comprising Neiguan (PC6), Sanyinjiao (SP6), Shuigou (GV26), Jiquan (HT1), Chize (LU5) Weizhong (BL40) and Fengchi (GB20) has been proved to be effective in curing patients with cerebrovascular lesion and subsequent disabled state [9–11]. Selection of the 7 main acupoints was based on the TCM theory. Sterile acupuncture needles (Huatuo, Suzhou Medical Instruments Factory, Suzhou, China), with a diameter of 0.25–0.30mm, were used in the trial. Once a characteristic aching and tingling sensation (known as “DeQi” meaning “obtained essence”) was elicited, the needle would be removed. Apart from traditional acupuncture treatment, the TG received the stimulation of surface projection zone of decussation of pyramid, which located at the junction between Yuzhen (BL9) and Tianzhu (BL10), and four equidistant points were chosen. Needles were inserted horizontally 15mm. After getting the needle sensation, the needle would be kept in situ for 20min. Treatment in the two groups should be performed once daily for 30days. Adverse reactions that occurred during acupuncture sessions were reported to the principal investigator, who would decide whether the trial should be terminated. Patients who had defaulted for 3 times would be treated as having dropped out of the trial. Causes of death and other reasons for withdrawal were also recorded. 2.4. Measurements Baseline characteristics and co morbidity of the enrolled patients, impairments and complications were all recorded. The outcome measures were assessed at baseline and after the intervention (within 3days after acupunctural treatment). Our test battery consisted of four measurements including the modified Ashworth scale (MAS), Fugl–Meyer Assessment (FMA), Barthel Index (BI), and the electromyographic activity of the affected extremity. Main outcome measure was the difference in MAS, FMA, BI, and EMG between arms. Predefined secondary outcome was the comparisons
2.4.2. Fugl–Meyer assessment (FMA) of motor performance FMA is a well-validated instrument assessing motor recovery after stroke, and has been widely used for both clinical and research purposes [15,16]. 2.4.3. Barthel index (BI) BI is a validated and widely used instrument to measure disability in ADL [17,18]. It has a total BI score of 100. The severity of disability is classified as mild (BI z 75), moderate to severe (20 b BI b 75), and very severe (BI V 20). 2.4.4. Electromyography (EMG) The electromyography system (Keypoint, DADTEC Biomedical Inc., Denmark) was used to perform nerve stimulation and reflex recording, before and after the 30-day treatment. The skin resistance overlying the abductor hallucis and extensor digitorum muscle were made as minimal as possible by shaving the area and brushing it with alcohol. The muscle responses were recorded through two silverchloride EMG electrodes, 9mm in diameter, coated with conducting cream. F-waves were evoked using a rectangular voltage pulse, 0.5ms in duration, by the stimulator. The stimulator was placed over the distal to the peroneal nerve and median nerve. The F-wave parameters were recorded and the F/M ratio was calculated by dividing the mean value of 10 F-waves by the mean value of 3Mresponses. 2.5. Statistical analysis For this pilot study, recruitment was limited by administrative factors. Therefore, it was projected that 120 eligible participants could be recruited and treated. The results were presented as mean ± SD. χ2 test, t-test and Wilcoxon test were used to compare the demographic characteristics and other variables of the 2 groups where appropriate. A value of P b 0.05 was considered significant. Statistical analysis was performed with SPSS version 10.0 (SPSS Inc., Chicago, Illinois, USA). 3. Results A total of 131 Chinese patients were enrolled and randomized to treatment group (n = 67) and control group (n = 64) in the present study. Patient baseline characteristics were comparable between the two groups (Table 1). No significant differences were found between the two groups for age, gender, stroke type, or time from stroke onset to be randomized (all Ps N 0.05). Among all the patients, no adverse effects were caused by the acupuncture treatment. Eleven patients dropped out during the trial, accounting for a 9% dropout rate. There were no deaths or protocol violators during the trial. Among the 11 dropouts, 3 patients had recurrent stroke; 6 defaulted on treatments; and 2 patients withdrew because they could not be discharged within the defined period because of a social problem. There was no statistical difference in dropouts between the 2 groups (Fig. 1).
J.-G. Zhao et al. / Journal of the Neurological Sciences 276 (2009) 143–147 Table 1 Baseline characteristics of the spastic hypertonia patients Characteristics
Treatment group (n = 67) Control group (n=64)
Age, y (mean ± SD) Gender Male Female Duration(since stroke), m (mean± SD) Stroke type Infarct Hemorrhage
58.50 ± 11.60
60.27 ± 11.71
52 15 16.34 ± 6.09
48 16 16.76 ± 6.89
49 18
51 13
Table 2 summarizes the MAS, FMA and BI baseline, post-treatment and change scores for stroke patients with spastic states. A modified Ashworth scale was used to evaluate the muscle tone of the main joints. Overall, the average (±SD) upper extremity Ashworth score significantly decreased, from 3.08 ± 0.77 at baseline to 1.82 ± 0.65 after acupuncture intervention (wrist joint, P b 0.05), and from 2.72 ± 0.59 baseline to 1.32 ± 0.71 after acupuncture intervention (elbow joint, P b 0.05). No significant baseline difference was observed in average upper extremity Ashworth score between treatment group and control group (P N 0.05). However, there were significant differences noted between the treatment group and control group after administration (P b 0.05). Lower extremity treatment responses were similar to upper extremity responses. The average (±SD) lower extremity Ashworth score significantly decreased, from 2.30 ± 0.59 at baseline to
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1.15 ± 0.48 after treatment (knee joint, P b 0.05), and from 3.02 ±0.68 at baseline to 1.67 ± 0.71 after treatment (ankle joint, P b 0.05). No significant baseline difference was observed in average lower extremity Ashworth score between treatment group and control group (P N 0.05). However, there were significant differences noted between the treatment group and control group after administration (P b 0.05). Furthermore, examination of the changes in MAS scores after treatment revealed that compared to the control group the improvement was significantly greater in the treatment group (all Ps b 0.05). At baseline, no differences between the two groups were found for the FMA or BI score. We found that there were significant differences between pre-treatment and post-treatment for the scores of FMA (upper extremity), FMA (lower extremity), FMA (total) and BI (P b 0.05, for all) in both treatment group and control group. In fact, both groups showed similar improvement in FMA (upper extremity) and FMA (lower extremity). Only the improvements of FMA (total) and BI were better in treatment group than in control group. However, as with the functional improvement analysis, there were statistically significant differences between the control and treatment groups when comparing the change scores for both the total and subscale FMA (P b 0.05, for all) (Table 2). In addition, Table 2 summarizes the EMG baseline and posttreatment activities for spastic patients. The F/M ratios of upper extremity of the two groups between pre-treatment and posttreatment were significantly different (P b 0.05). The F/M ratio of lower extremity also decreased significantly as compared to the pre-
Fig. 1. Trial flow diagram.
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Table 2 Outcome changes between the two groups Outcome measure muscle tone (wrist joint) muscle tone (elbow joint) muscle tone (knee joint) muscle tone (ankle joint) FMA (upper extremity) FMA(lower extremity) FMA (total) BI EMG (upper extremity) F-wave amplitude (mean) F-wave amplitude (max) F/M ratio EMG(lower extremity) F-wave amplitude (mean) F-wave amplitude (max) F/M ratio
Treatment group
Control group
Baseline
After treatment
Change
Baseline
After treatment
Change
3.08 ± 0.77 2.72 ± 0.59 2.30 ± 0.59 3.02 ± 0.68 34.12 ± 3.96 17.63 ± 1.68 51.75 ± 4.97 41.83 ± 8.88
1.82 ± 0.65*△ 1.32 ± 0.71*△ 1.15 ± 0.48*△ 1.67 ± 0.71*△ 42.80 ± 3.74* 22.90 ± 1.98* 65.70 ± 4.91*△ 65.25 ± 8.95*△
1.27 ± 0.69△ 1.40 ± 0.59△ 1.15 ± 0.55△ 1.35 ± 0.58△ 8.73 ± 2.19△ 5.35 ± 2.21△ 14.08 ± 3.73△ 23.92 ± 5.76△
2.92 ± 0.70 2.52 ± 0.64 2.12 ± 0.64 3.02 ± 0.65 34.67 ± 3.08 17.75 ± 1.74 52.42 ± 3.72 39.83 ± 8.13
2.65 ± 0.93* 1.90 ± 0.78* 1.70 ± 0.81* 2.93 ± 0.86 41.68 ± 3.44* 22.22 ± 1.68* 63.90 ± 4.55* 59.92 ± 8.16*
0.27 ± 0.48 0.68 ± 0.57 0.45 ± 0.50 0.15 ± 0.51 7.02 ± 1.91 4.47 ± 1.36 11.48 ± 2.94 20.25 ± 5.71
0.37 ± 0.14 0.54 ± 0.36 0.10 ± 0.07
0.25 ± 0.08*△ 0.33 ± 0.13*△ 0.05 ± 0.04*△
0.40 ± 0.24 0.56 ± 0.22 0.12 ± 0.08
0.34 ± 0.19* 0.57 ± 0.29 0.09 ± 0.06*
0.29 ± 0.17 0.55 ± 0.27 0.12 ± 0.11
0.17 ± 0.07*△ 0.35 ± 0.21*△ 0.05 ± 0.03*△
0.33 ± 0.16 0.65 ± 0.27 0.14 ± 0.07
0.31 ± 0.15 0.52 ± 0.20* 0.10 ± 0.05*
*p b 0.05, compared with pre-treatment; △p b 0.05, compared with control group.
treatment ratio (P b 0.05). However, the improvements of the F/M ratios were better in treatment group than in control group. 4. Discussion Spasticity has been defined as a motor disorder characterized by a velocity-dependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as a component of the upper motoneuron syndrome [19,20]. The increased muscle tone may be noted in all affected synergistic muscle groups following a stroke, thereby reducing functional motor activities. Although there are numerous approaches to the treatment of spasticity, many patients are still unable to find a satisfactory method of managing their spasms with acceptable side effects. In the present study, the effectiveness of acupuncture on spasticity was evaluated by independent, blinded assessors for tone, motor performance, daily activities and electromyography. Our results have shown significant improvement in muscle tone, motor impairment, and disability in patients receiving combined acupuncture treatment as compared with the control. Some previous studies [21,22] have also shown the effect of acupuncture treatment on the reduction in spasticity using clinical measurements. The clinical measurement using MAS scores showed a similar reduction like the quantitative measurement in our study. Acupuncture may change the motoneuron activity and/or change synaptic transmission from muscle afferent terminals to spinal motoneurons, presumably mediated by presynaptic interneurons, and change intrinsic motoneuron properties, including membrane input resistance or membrane receptor responsiveness to released transmitters [23]. A recent study showed that acupuncture led to immediate and short-term plastic brain reorganization in comparison to needling at non-acupuncture points in healthy subjects [24]. Hence, acupuncture treatment for stroke motor impairment can be more efficacious than traditional approaches, which focus on impairment. The importance of sensory stimulation in stimulating the brain and facilitating recovery has been shown with functional MRI and is likely the physiological underpinning for the use of acupuncture for facilitating motor recovery. Acupuncture has also been shown to suppress the amplitude of somatosensory evoked potentials in both humans and animals [25]. The junction between Yuzhen (BL9) and Tianzhu (BL10) in Bladder meridian of foot-taiyang is the surface projection zone of decussation of pyramid, and is spatially correlated with the areas of the motor tracts controlling liberomotor function of specific parts of the body, although the cranial bone separates them and the focus lies in the deeper portion of the brain. Stimulating the acupoints along these
meridians can facilitate the restoration of motor impairment and disability. Furthermore, there have been classical acupuncture treatments in the body acupoints (including the head) for strokes, which mainly adopted activating brain and regaining consciousness needling method, which has been proved to be effective in improving a disabled state [9–11]. These suggest that there are at least two pathways, for example afferent and efferent connecting with the damaged parts of the brain. This appears to show some parallelism with rehabilitation therapy involving stimulation and motivation [26]. It is likely that acupuncture is much more direct and effective. The characteristics of spasticity could be related to changes in neurophysiology and muscle properties. The alterations in F-wave parameters in spasticity are more precise for assessment of alpha motoneuron excitability than the well known T and H-reflexes [27– 29]. In the present study, we used the F/M ratio to measure changes in motor neuron excitability, which made changes in the mechanism of spasticity clearer from the neurological standpoint. We found that the F-wave in amplitude (mean and maximal) and the F/M ratios significantly decreased after acupuncturing surface projection zone of decussation of pyramid (p b 0.05). This result indicated that the acupuncture treatment could inhibit the neuron excitability in patients with spastic hypertonia from stroke. A few comments about our method of design and our study limitations deserve mention. First, one potential limitation of the study is that as a pilot study, no power analysis was provided in this study, which lowered the statistical power of the study to a certain extent. Second, another limitation is that many variables were assessed in the present study and did not have a primary outcome measure. Combined clinical and neurophysiologic evaluation of acupuncture response among stroke patients with spastic states has not been previously described. Thus, our primary objective was to evaluate changes in the Ashworth Scale, Fugl–Meyer Assessment, Barthel Index, and EMG activity after acupuncture treatment for spastic hypertonia resulting from stroke. Third, although the study evaluators were blinded to the treatment assignment, the patients were not blinded. Therefore, one of the limitations of this pilot study is that we did not measure the effect of patient expectation. Furthermore, the follow-up data after treatment were not available. Although the initial study plan considered a long-term follow-up, limited resources did not permit patient post-treatment clinic or home visits for assessing spastic states and motor function. Finally, no sham acupuncture was used in this pilot study. Therefore there was no guarantee that the placebo effect of the acupuncture treatment had been removed completely from the results, even though taking the routine treatment group as control in the present study.
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