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Poursaeed F, Tahan N, Dehghan Manshadi F, Akbarzade Bagheban A R. Effects of Extracorporeal Shockwave Therapy on Clinical and Neurophysiological Indices of Spasticity Inpatients With Upper Motor Neuron Lesions: A Systematic Review and Meta-analysis. jrehab 2021; 22 (1) :28-47
URL: http://rehabilitationj.uswr.ac.ir/article-1-2836-en.html
1- Department of Physical Therapy, School of Professional Studies, Northeastern University, Boston, Massachusetts, USA.
2- Department of Physiotherapy, School of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran. , nahidta2431@gmail.com
3- Department of Physiotherapy, School of Rehabilitation, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
4- Department of Biostatistics, Proteomics Research Center, School of Allied Medical Sciences, Shahid Beheshti University of Medical Sciences,Tehran, Iran.
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pasticity is one of the symptoms of upper motor neuron damage that usually appears after a period of muscle relaxation as an increase in speed-dependent resistance during patio movement with the intensification of tendon reflexes [1]. This movement disorder is commonly seen in patients with cerebral palsy, hemiplegia, multiple sclerosis, and spinal cord injuries. Neural and non-neural mechanisms can lead to increased resistance to patio movement in upper motor neuron injury. Nervous mechanisms are due to the removal of inhibition of the cortical-spinal pyramidal pathway and extra-pyramidal pathways (rubrospinal and vestibulospinal) from the brain stem and spinal cord [6], but non-neural mechanisms are associated with muscle stiffness and high levels of collagen and connective tissue in the spastic muscle [2]. Prolonged spasticity can cause changes in the structural properties of the involved muscle and adjacent muscles in a short time or muscle fibrosis, which causes abnormal control of the position of the limb and as a result, movement disorder in the limb [7].
Pharmacotherapy and rehabilitation interventions, especially those that focus on connective tissue flexibility, are non-invasive treatments to reduce spasticity [8]. Shock Wave Therapy (SWT) is one of the most promising methods to reduce spasticity today, but it has not yet been used as a common treatment [9, 10]. Shockwaves are high-energy sound waves (100 MPA) that are produced in a very short time (10 microseconds) and at high pressure [11]. Shockwaves have been reported in the treatment of orthopedic lesions, such as non:union: in long bones, inflammation of the plantar fascia, calcified shoulder tendonitis, inflammatory tendon diseases, and spasticity [12]. SWT can be used in both focal and radial forms. Focal shockwaves are generated by electromagnetic, hydroelectric, and piezoelectric methods, while radial shockwaves are generated pneumatically. In addition, the penetration depth of radial shockwaves is less than focal shockwaves [11].
So far, no precise mechanism has been proposed to justify the effects of SWT in reducing spasticity. A group of studies believes that “shockwave” shock waves can have a direct effect on fibrosis muscles and non-reflex components of spastic muscle. This mechanism of shock wave effect can be explained by the results of some studies on the positive effects of SWT on the tendon and musculoskeletal problems in patients with hypertension [13]. Some studies have shown that shockwaves at the muscle level can alter the sensory flow of the muscle, which by acting on free nerve terminals, reduces muscle excitability at the spinal cord level and ultimately reduces spasticity [14]. Studies on non-human specimens have shown that shockwave delays neuromuscular transmission at the neuromuscular junction and is a possible mechanism for reducing muscle pain and tonicity [15]. There are various clinical tools and neurophysiological methods for assessing spasticity. Evaluation of neurophysiological responses of spastic muscle is possible by examining tendon reflex, F wave, M wave, and Hoffman reflex [1617]. 
The Ashworth scale is a common tool for the clinical assessment of spasticity, which is based on the assessment of patio joint resistance [18]. Most studies on the effects of SWT on muscle tone have used the clinical scale of Ashworth or biomechanical scales and only in two studies, evaluation was performed by measuring ultrasound of muscle architecture [1920].
Due to the need for spasticity treatment in neurological patients and because in clinical studies on the effect of SWT on the reduction of spastic muscle tone, no specific treatment protocol has been used, and also because systematic reviews and meta-analysis are tools for summarizing the available evidence accurately and reliably [21], the present study was done to analyze the available clinical trial studies on the effectiveness of SWT in reducing spastic muscle tone at the time immediately and three months after shockwave application in patients with upper motor neuron lesions.
Materials and Methods
In this study, databases, including PubMed, ISI Web of Science, ScienceDirect, MEDLINE, Scopus, and Google Scholar search engine were searched using the keywords of muscle hypertension or spasticity, cerebral palsy, stroke, multiple sclerosis, and shockwave therapy. All clinical trials published from January 2005 to January 2020 were enrolled. Studies examining spasticity with a modified Ashworth Scale (MAS) and/or neurophysiological parameters in patients with stroke, cerebral palsy, and multiple sclerosis were selected. Two independent researchers searched and reviewed eligible studies in terms of inclusion criteria and assessed the methodological quality of selected studies.
First, the abstracts were reviewed, and then, the full text of the articles was reviewed based on the inclusion criteria. Studies unavailable in their full-text form, those published in a non-English language, and studies, in which shockwave had been used for purposes other than spasticity treatment were excluded from the study. Articles with the following characteristics were selected for meta-analysis: 1. Original research articles; 2. Clinical trial studies with a control group or pre-test/post-test design; 3. Studies using the MAS to assess spasticity (at least two times, one immediately after the intervention and the other, 3 months after SWT; and 4. studies using neurophysiological indicators to assess spasticity. The methodological quality of the selected studies was assessed using the Downs and Black Scale. This scale consists of 27 items and is designed to evaluate the methodological quality of random and non-random studies [22].
Statistical analysis
The difference between the means was considered as the effect size in the scores of the joint Ashworth scale before, immediately, and three months after the intervention for meta-analysis. Another meta-analysis was performed on the differences in means in neurophysiological indices before and after the intervention. Heterogeneity was assessed (presence or absence of homogeneity) between studies using the I² index. Due to the confirmation of heterogeneity of studies (P>50%) using the Ashworth scale and neurophysiological indices, the random-effects model of the meta-analysis was used. This model shows the mean difference of each study and the value of the combined mean difference as well as their confidence intervals. Emission bias was also assessed using Egger’s test. Data were analyzed using STATA software version 11. Values ​​of p less than 0.05 were considered statistically significant.
Using the above keywords, a total of 98 articles were selected in the first stage, which after deleting 31 unrelated articles and 43 duplicate articles, 24 articles remained. Among these articles, the full text of two articles was not found, and three articles were clinical trials on animals. The other five articles were omitted for the following reasons: three studies did not report mean values ​and Standard Deviation (± SD) and two articles used the MAS. A total of 14 articles were included in the systematic review and meta-analysis. The flowchart of the selection process of studies is shown in Figure 1
All related studies were analyzed in terms of patient characteristics, treatment sessions, muscles examined, intensity and number of treatment pulses, evaluation methods, and finally the results obtained (Table 1). 

The quality of the studies entered varied. Based on the Downs and Black score, one excellent study, two good studies, seven relatively good low-quality, and four low-quality studies were determined. The mean score of methodological quality in all studies was 17 and in the range of 10-27. Table 1 shows the qualitative scores of all studies.
Systematic review findings
As shown in Table 1, the observed differences between the articles are in the type of disease, the number of treatment sessions, the muscles examined, and the energy applied. Out of 14 articles included in the study, 11 articles had examined the effect of shockwave in stroke patients, one study in multiple sclerosis patients, and 3 studies in cerebral palsy patients, which is probably due to the higher prevalence of stroke patients in the community. The number of treatment sessions in 7 studies was one and in other studies, the duration of treatment lasted between 3 and 6 weeks. The highest number of sessions was found in the study by Wang et al. with one session of treatment per week for 3 months and a total of 12 sessions [23]. In terms of the duration of the therapeutic effects of shockwave, Moon et al. concluded that the effect of SWT decreases over time [24]. While studies by Manganotti et al. [25] and Amelio et al. [26] confirmed the long-term effects of shockwave. In terms of examined muscles, the gastrocolic muscle had been studied in eight studies, wrist and finger flexor muscles in 5 studies, and biceps muscle in one study. The difference in the parameters of the shock wave device in terms of energy intensity used varied from 0.03mJ/mm2 to 0.32mJ/mm2. In most studies, low energy intensities had been used in the treatment, but no reason had been provided by the researcher in choosing the intensity of application.
A total of 12 studies had evaluated the effect of SWT on the scores of the MAS. Among these articles, 3 studies had evaluated the effect of SWT three months after treatment using this scale [252627]. Manganotti simultaneously evaluated two groups of forearm flexor and intrinsic hand muscles [25]. In his study, Wang evaluated the right and left gastrocnemius muscles separately [23]. Li examined the intrinsic muscles of the hand in 2 groups and the forearm flexor muscles in 2 groups [27].
Meta-analysis findings
A. Analysis of the results of studies included in the meta-analysis by examining the effect of shockwave on the scores of the modified Ashworth scale:
A total of 18 interventions that evaluated the effect of shockwave on the MAS scores before and after treatment and 7 studies that examined the effect of shockwave on the MAS scores before and three months after SWT were included in the meta-analysis.
The results of the meta-analysis showed a significant decrease in the MAS immediately after treatment; however, the Ashworth scale scores decreased by 1.38 with a 95% confidence interval. [I² = 100%; P<0.001, SDM=1.38 With 95%CI: (0.80, 1.87)]. Figure 2 of the Forest Plot diagram shows the extent of changes in the Ashworth scale before and immediately after SWT in general and separately for all studies. 

With a confidence interval of 95%, the difference between the mean before and immediately after the Ashworth scale was equal to 0.80 and 1.87, respectively, which shows that the mean of the Ashworth scale before and immediately after the intervention was significantly different.
The results of the meta-analysis also showed that three months after the intervention, the scores of the MAS decreased significantly. [I² = 100%, p <0.001, SMD = 1.13 with 95%CI: (0.50, 1.76)] . Figure 3 of the Forest Plot diagram shows the rate of changes in the scale of Ashworth scale before and 3 months after. 
SWT in general and separately for all studies
With a 95% confidence interval, the mean difference in comparison between before and 3 months after the Ashworth Scale was equal to 0.50 and 1.76, respectively, which shows that the mean Ashworth Scale before and 3 months after the intervention was significantly different.
B- Analyzing the results of studies included in the meta-analysis by examining the effect of shockwave on the Hoffman reflex/motor response (H/M) ratio:
Four studies with a total of 120 patients had evaluated the effects of SWT on the H/M ratio. Figure 4 shows the Forest plot diagram of changes in H/M ratio before and after SWT in general and separately for all studies. 

With a 95% confidence interval, the mean difference in comparison with before and after the ratio of H/M was 0.54 and 2.73, respectively, which indicates that the mean index of the H/M ratio before and after the intervention was not significantly different.
Discussion and Conclusion
In general, one of the most important goals of meta-analysis studies is to solve problems caused by controversial results of previous studies. In these studies, by combining several studies with specific characteristics, the sample size increases, which reduces the confidence interval of measurements. As a result, a valid result can be presented from previous studies [28].
The results of the present study showed that the degree of the Ashworth scale decreased significantly after shockwave application. In this meta-analysis, the effects of shockwave on the reduction of spasticity at follow-up (3 months after treatment) were also significant. So far, several systematic reviews and meta-analyses have been performed to evaluate the effect of SWT on spasticity in patients with upper motor neuron lesions. However, no study has been performed on the simultaneous evaluation of the effects of SWT on the clinical and neurophysiological symptoms of spasticity in patients with upper motor neuron lesions with different etiologies.
The results of other review studies that have examined the effect of SWT on the severity of spasticity are consistent with the results of the present study. Lee et al. (2014) reviewed 5 studies (3 studies in patients with partial paralysis and 2 studies in patients with cerebral palsy) and stated that the MAS score immediately and 4 weeks after SWT significantly improved compared with the baseline values ​​[29].
Guo et al. (2017) in their systematic review and meta-analysis and based on data from 6 studies on stroke patients, analyzed the effects of SWT in reducing spasticity and reported significant differences between baseline values ​​of the Ashworth scale immediately and 4 weeks after treatment [30].
Xiang et al. (2018) in their systematic review and meta-analysis of 8 clinical trials on stroke patients reported that there is a high level of evidence to confirm the positive effects of SWT in reducing spasticity immediately after treatment. Ashworth, Tardio scale, H/M ratio, and joint range of motion were analyzed in this study [31].
A systematic review and meta-analysis conducted in 2020 by Cabanas-Valdés et al. obtained similar results to the results of the present study. In two separate articles, the author examined the effects of SWT on reducing spasticity of the lower and upper limb muscles in patients with partial paralysis and reported that SWT has significant effects on improving the MAS, range of motion, and Fugl Meyer criteria in the short and long term [10].
Another finding of this study showed was no significant changes in alpha motor neuronal excitability (H/M ratio) in patients with upper motor neuron lesions after SWT.
This finding contradicts the findings of a review study by Guo et al. [30]. A noteworthy point in their study was that the effects of SWT on H/M ratio were assessed only by meta-analysis of one study, while in the present study meta-analysis was performed according to the inclusion criteria of 4 articles. Therefore, this could be a justification for the discrepancy between the findings of the present study and their study.
In this context, based on inclusion criteria, four articles that had investigated the immediate effects of spastic muscle SWT on the H/M ratio were included in this study. Radinmehr et al. (2016) reported that by performing a shockwave session on the gastrocnemius muscle of 12 stroke patients and recording the H/M ratio immediately and one hour after treatment, despite the reduction of the H-reflex latency, no change in the H/M ratio was observed [32]. Shon et al. (2011) in their study on 10 stroke patients reported that one session of SWT on the gastro-soleus muscle did not show significant changes in the H/M ratio compared with before treatment [33]. Gawad et al. (2015), observed a significant decrease in the H/M ratio after 3 sessions of treatment in patients with cerebral palsy [34]. Marinelli et al. (2015) reported that 4 sessions of SWT could significantly reduce electrophysiological parameters in patients with multiple sclerosis [35].
A significant consideration in studies that have examined the H/M ratio of spasticity is the time interval between the onset of upper motor neuron lesions. However, the H/M ratio is a reliable measure of the excitability of upper motor neurons. However, studies using the H/M ratio to assess spasticity did not indicate the onset of upper motor neuron lesions in patients with the disease. Hiersemenzel et al. (2000) reported that the H/M ratio reaches its maximum value at least 2 to 6 months after the onset of upper motor neuron lesion and then, remains constant [36]; thus, the H/M ratio may not be stable before this time. Therefore, it seems that the evaluation of patients in terms of the H/M ratio concerning the time of onset of the complication is an important factor in the evaluation result and can affect the results of the study. Therefore, it is recommended that studies that use this ratio to evaluate the effects of different therapies on spasticity consider the time elapsed since the onset of upper motor neuron lesion. Although the results of all studies confirm the positive effects of SWT in reducing spasticity based on the Ashworth scale, it seems that many questions must be answered before this method can be recommended to patients as a common method of reducing spasticity. 
First, to determine the independent effect of shockwave on spasticity, it is necessary to limit the use of any other treatment that can affect the severity of spasticity to avoid confusion in the expression of results. For example, Gawad et al. (2015) in their study used exercise therapy protocol in the control and treatment groups along with SWT [34]. Wang et al. (2016) used Chinese massage and electrical stimulation along with SWT [23]. Sohn et al. (2011) used antispasmodics with a shock wave in their study [33]. On the other hand, differences in the number of treatment sessions, treatment session intervals, energy density and number of shocks applied, and follow-up time need to be examined more closely. The existence of these differences significantly increases the level of heterogeneity in studies. Therefore, because of the lack of adequate data from the main articles for meta-analysis of the above variables in any of the reviews and meta-analyses, the effect of SWT with different shocks and intensities and the duration of different treatments was not analyzed. Therefore, in future studies, it is recommended to conduct clinical trials considering the following items: 1. Patients should be divided into different groups based on the characteristics of the shock wave, the number of treatment sessions, and the duration of follow-up; 2. The samples should be matched in terms of the Ashworth scale; 3. Factors related to spasticity (type of upper motor neuron lesion and even type of stroke) should also be considered in the selection of patients.
One of the limitations of this study is the small number of well-designed clinical trials, considering that the mechanism of effectiveness of SWT on spasticity is not yet fully understood, and on the other hand, there is no integrated protocol in the treatment of spasticity by SWT; thus, more trials with appropriate designs are needed in the future.
The results of this review study showed that SWT is a non-invasive method that can be easily used in spastic muscles of the lower and upper limbs in patients with upper motor neuron lesions and has beneficial effects on improving the clinical scale of spasticity assessment. Because there is still no single instruction for treating patients in terms of the number of treatment sessions, energy intensity, and several shocks applied, and on the other hand, none of the studies provided a documented reason for choosing the number of sessions and pulse intensity as a common method of reducing spasticity, conducting high-quality randomized clinical trials is suggested to analyze the factors affecting SWT on spasticity.

Ethical Considerations
Compliance with ethical guidelines

All ethical principles are considered in this article. 

This article has been done with the financial support of the Vice Chancellor for Research and Technology of Shahid Beheshti University of Medical Sciences.

Authors' contributions
Conceptualization and project management: Nahid Tahan; Research: Nahid Tahan and Farideh Dehghan Manshadi; Data collection: Nahid Tahan and Fereshteh Poursaid; Editing and writing – review & editing: All authors; Statistical analysis: Alireza Akbarzadeh Baghban.

Conflict of interest
The authors declared no conflict of interest.

The authors thank the Vice Chancellor for Research and Technology of Shahid Beheshti University of Medical Sciences.

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Type of Study: Review | Subject: Physical Therapy
Received: 24/09/2020 | Accepted: 15/12/2020 | Published: 1/04/2021

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