Figures
Abstract
Objective
The aim of this meta-analysis was to evaluate the effect of whole-body vibration training on lower limb motor function in children with cerebral palsy in randomized-controlled trials (RCTs).
Methods
Two independent reviewers systematically searched the records of nine databases (PubMed, Cochrane, Web of Science, EMBASE, CNKI, etc.) from inception to December 2022. Tools from the Cochrane Collaboration were used to assess risk of bias. Standard meta-analyses were performed using Stata 16.0 and Revman 5.3. For continuous variables, the arms difference was calculated as the weighted mean difference (WMD) between the values before and after the intervention and its 95% confidence interval (95% CI).
Results
Of the 472 studies identified, 13 (total sample size 451 participants) met the inclusion criteria. Meta-analysis showed that WBV training could effectively improve GMFM88-D [WMD = 2.46, 95% CI (1.26, 3.67), P<0.01] and GMFM88-E [WMD = 3.44, 95% CI (1.21, 5.68), P = 0.003], TUG [WMD = -3.17, 95% CI (-5.11, -1.24), P = 0.001], BBS [WMD = 4.00,95% CI (3.29, 4.71), P<0. 01] and the range of motion of ankle joint and the angle of ankle joint during muscle reaction in children with cerebral palsy. The effect of WBV training on 6MWT walking speed [WMD = 47.64, 95% CI (-25.57, 120.85), p = 0.20] in children with cerebral palsy was not significantly improved.
Conclusion
WBV training is more effective than other types of conventional physical therapy in improving the lower limb motor function of children with cerebral palsy. The results of this meta-analysis strengthen the evidence of previous individual studies, which can be applied to the clinical practice and decision-making of WBV training and rehabilitation in children with cerebral palsy.
Citation: Cai X, Qian G, Cai S, Wang F, Da Y, Ossowski Z (2023) The effect of whole-body vibration on lower extremity function in children with cerebral palsy: A meta-analysis. PLoS ONE 18(3): e0282604. https://doi.org/10.1371/journal.pone.0282604
Editor: Nili Steinberg, The Wingate College of Physical Education and Sports Sciences at the Wingate Institute, IL, ISRAEL
Received: April 21, 2022; Accepted: February 18, 2023; Published: March 10, 2023
Copyright: © 2023 Cai et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: CP, cerebral palsy; WBV, whole-body vibration; RCTs, randomized controlled trials; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-analysis; GMFM88-D/E, Gross motor function measurement-88 in Zone D/E; 6MWT, 6-min walk test; TUG, Timed Up and GO test; BBS, Berg Balance Scale; Ankle-ROM, The range of motion of ankle joint; Ankle-R1/R2, The angle of ankle (1/2) joint during muscle reaction; WMD, weighted mean difference; 95% CI, 95% confidence intervals; BoNT-A, Botulinum toxin type A; WBVAO, whole-body vibration combined with action observation
Introduction
Cerebral palsy (CP) is long-standing dyskinesia of motor posture caused by chronic brain injury to the developing fetus or infant [1], and it frequently results in limited motor abilities in children, of whom spastic cerebral palsy is the most common [2, 3]. More than 50% of children have lower limb movement disorders, such as lower limb muscle contracture, ankle stiffness and deformity, hip and knee flexion when standing and walking, sharp foot crossing, etc., which seriously affect the normal growth development and motor function of children [1–4].
Whole-body vibration (WBV) training method is a new non-traditional training method [5], through external intervention, which allows subjects to generate adaptive responses to vibration stimulation through a specially designed vibration platform [6, 7]. Currently, it is used as a clinical treatment to increase muscle strength, usually involving a series of static or dynamic movements in a standing posture on a vibrating pad. It was originally used by elite athletes to increase speed and strength [8]. In recent years, this method has been widely popularized and applied in many fields abroad, and has also achieved some positive therapeutic and training effects. WBV appears to be a promising adjunct to conventional treatment involving CP patients. According to the studies evaluated by these authors, WBV may help to improve walking ability, walking speed, overall mobility, muscle mass and force production, and reduce spasticity [8]. Furthermore, some authors concluded that horizontal WBV training should be included in rehabilitation programs for children with CP, as it can improve their physical performance without harmful effects [9].
Studies have also confirmed that WBV training can improve the lower limb function of children with cerebral palsy [10, 11]. However, due to the various experimental design protocols of relevant studies regarding the application of WBV training in lower limb rehabilitation of cerebral palsy patients at this stage, the small number of study subjects and the uneven quality of the comprehensive review literature often lead to conflicting final study conclusions. Therefore, it is necessary to comprehensively and systematically evaluate the effect of WBV training on the lower limb rehabilitation of children with cerebral palsy.
This study intends to select randomized controlled trials on the impact of WBV training on lower limb motor function of children with cerebral palsy and evaluate the results of the consistent study by meta-analysis. To comprehensively and quantitatively evaluate the improvement effect of WBV training on lower limb function indexes of children with cerebral palsy, and to provide more reliable basis for clinical practice and decision-making of WBV training and rehabilitation of children with cerebral palsy.
Methods
Literature search
The research team conducted the meta-analysis in compliance with the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) [12]. Two researchers independently performed a comprehensive literature review. The reviewed databases included Web of Science, PubMed, Embase, Scopus, Cochrane, EBSCO, CNKI, Wanfang Database and VIP, which were systematically searched to identify relevant articles up to December 15, 2022. Additionally, references were incorporated retrospectively into the literature to supplement access to the relevant literature. The combination of free words with theme words was performed in this study.
Search strategies were developed using Boolean logical operators, truncates, etc. for comprehensive searches. Search terms were used including: whole-body vibration, WBV, Cerebral Palsy, CP, Dystonic-Rigid Cerebral Palsy, Mixed Cerebral Palsy, Monoplegic Infantile Cerebral Palsy, Quadriplegic Infantile Cerebral Palsy, Rolandic Type Cerebral Palsy, Congenital Cerebral Palsy, Little Disease, Spastic Diplegia, Monoplegic Cerebral Palsy, Athetoid Cerebral Palsy, Dyskinetic Cerebral Palsy, Atonic Cerebral Palsy, Hypotonic Cerebral Palsy, Diplegic Infantile Cerebral Palsy, Spastic Cerebral Palsy, Child, Lower Limb, Membrum inferius, Lower Extremity.
Using PubMed as an example, see Table 1 for specific search strategies (see S1 Table for the rest of the search strategies).
Eligibility criteria
Primary outcomes
(1) Gross motor function measurement-88 in Zone D (GMFM-88-D)
GMFM-88 is applicable for evaluating gross motor function in cerebral palsy, with appropriate reliability and validity. It encompasses the evaluation of five functional areas A-E, with each evaluated individually or in combination. A total of 13 items are found in Zone D, reflecting standing ability [13, 14].
(2) Gross motor function measurement-88 in Zone E (GMFM-88-E)
A total of 24 items exist in Zone E, reflecting the ability to walk, run and jump [14]. According to the completion level, each item scores 0–3 points [14]. A greater functional level brings about a higher score [15].
(3) Six-min walk test (6MWT)
The 6MWT was utilized to assess the walking speed of participants. The child patient stood on the starting line and set the timer going as soon as walking. Patients walked back and forth as much as they could in the interval. During this period, the monitor could give verbal advice and encouragement. At the end of the test, the 6-min walking distances of patients were recorded [16, 17].
(4) Timed Up and Go test (TUG)
In the TUG test, participants wore ordinary shoes, sat on back chairs with armrests, and leaned on the back of chairs. They held hands on armrests, stood up from the back chair, and used walking aids if necessary. Child patients walked 3 meters forward with a usual walking gait, crossed the thick line or mark. Then they turned around and walked back to the chair. All patients sat down and leaned against the back of chairs. A stopwatch was used to record the time from the patient’s back leaving the chair back to their sitting again. The risk of falling during the test was recorded. The test was repetitively conducted 3 times, with data recorded to calculate and take the average value for analysis [18, 19].
Secondary outcomes
(1) Berg Balance Scale (BBS)
BBS was used to evaluate the balance function. Items totaled 14, with each scoring 0–4 points. A relatively high score represented greater balance ability [20, 21].
(2) The range of motion of the ankle joint (Ankle-ROM)
A joint protractor was mainly used to measure the range of motion (ROM) of the ankle joint. Also, ankle-ROM was divided into active and passive. Each measurement was performed 3 times, and the mean was recorded as ROM [22].
(3) The angle of ankle (1/2) joint during muscle reaction (Ankle-R1/R2)
Ankle-R1/R2-fast angle refers to the angle of jamming during rapid traction, recorded as angle 1 (R1); the slow angle refers to the full range of the joint motion under slow movement, recorded as angle 2 (R2) [11].
Exclusion criteria
(1) History of bone and joint diseases of lower limbs, orthopedic surgery and use of antispasmodic drugs.
(2) Severe cognitive, intellectual and hearing impairment.
(3) Studies focused on therapy for lower-limb motor function in children with cerebral palsy rather than WBV training.
(4) Obvious errors in the original research and test scheme (incomplete article content, etc.).
(5) Non-randomized controlled trials (review literature, repetitive published clinical trial literature and animal trial research literature).
(6) Incomplete literature for data reporting.
(7) Studies with insufficient data failing to interpret results.
Literature quality assessment and data extraction
Data extraction and management.
The literature review was screened separately by two scholars. Following the computer retrieval of major databases, titles and abstracts of all filtered articles were imported into the literature management software (EndNote X9 and Microsoft Excel). Duplicate literature was screened out. Titles and abstracts were checked to figure out articles unqualified for inclusion requirements. Finally, through full-text reading, literature meeting the criteria was sifted out. Any discrepancies during literature screening were solved by consulting relevant experts or talking to a third researcher. If numerous articles relevant to a study had been published, those with the most comprehensive experimental data and of outstanding consistency with inclusion criteria would be included in this study. Office program was used to sort out and analyze all the selected eligible literature in terms of basic literature information (title, author, and publication year), general information (patient age, gender, number of cases, etc.), experimental design (interventions), and outcome indicators. Literature with inconsistent outcome indicator units would be uniformly translated before data processing. When data were lacking in the literature, we would contact the original author by e-mail or phone to gather the necessary information. Fig 1 depicts the PRISMA flow chart for choosing literature.
Literature quality assessment.
The findings of a bias risk assessment adopting the approach provided by the Cochrane Handbook for System Reviews of Interventions Version 5.1.0 were presented in the chosen literature. Evaluation can be conducted by resorting to the randomization method, allocation of covert scheme design, blind method, and reporting of results data. Moreover, literature quality could also be assessed by verifying selective reporting of research results, other reasons of bias, etc. According to the results, “Yes” indicated the reasonable method or complete data and the low risk of bias; “Unclear” denoted unclear method and moderate risk of bias; “No” represented the incorrect method or incomplete data and high risks of bias. Finally, the examination findings were entered into the RevMan 5.3 program to generate a bias risk assessment chart.
Statistical analysis
Meta-analysis was performed using RevMan 5.3 and STATA 16.0 (STATA Corp, College Station, TX, USA). For continuous variables, the weighted mean difference (WMD) was used as the effect index, and each effect size was expressed with a 95% confidence interval (95% CI), P<0.05 indicates a statistically significant difference between the two groups. The I2 statistic was used to test the heterogeneity among different studies. When P>0.1 and I2≤50%, it means that there was good homogeneity among all studies, and the fixed effect model was used to combine the effect size. When P≤0.1 and I2>50%, it means that there was heterogeneity between the studies, and the random effect model was used to combine the effect size. The source of heterogeneity was identified, and sensitivity analysis was conducted by article by article elimination. If I2≤50% after deleting a single study, it was considered that the study might be the source of influencing the combined effect size, and it was excluded from the meta-analysis. In addition, The Begg’s and Egger’s tests were performed to assess publication bias. P<0.05 was statistically significant unless otherwise specified.
Results
Search results
The S1 Table contains the complete search methods. Fig 1 depicts the study selection procedure. The nine databases yielded a total of 472 studies (PubMed = 10, Cochrane = 20, Scoups = 238, Web of Science = 16, Wanfang Database = 6, CNKI = 7, VIP = 4, Embase = 10, and EBSCO = 161). Other records could not be found through other sources. 382 articles remained after duplicates were deleted; however, 339 records were further deleted after reading the titles and abstracts. For different reasons, 43 full-text papers were read in depth for eligibility, and 30 articles were removed. Finally, this meta-analysis comprised 13 papers [10, 11, 23–33].
General characteristics and quality evaluation of included studies
Literature characteristics.
Of the 13 articles in this meta-analysis, 13 reported the use of WBV training, 12 reported the use of conventional physiotherapy. One reported that Botulinum toxin type A (BoNT-A) injection was combined with conventional physiotherapy. One reported the use of whole-body vibration combined with action observation (WBVAO) training combined with conventional physiotherapy, and one reported that conventional physiotherapy was changed to passive stretching exercise. The patients included in the study were children with cerebral palsy, they need WBV training to observe the effect of this treatment on the motor function of lower limbs. All control groups were also children with cerebral palsy. Except for one control group with WBV training, the rest of the latter group of patients only received conventional physiotherapy without WBV training. The characteristics of the included articles are reported in Table 2.
Risk of bias of included literature.
The included studies were assessed for selection bias, performance bias, detection bias, attrition bias, and reporting bias. The word “random” was mentioned in all studies, with only one article mentioning “coin tossing”, one mentioning “simple randomization”, and three mentioning “random number table method”. Based on the method of randomization and concealment of allocation, all studies were determined to have a low risk of selection bias. Of the seven articles that described the evaluator blinding method, four had a low risk of detection bias and three had a high risk (as one person evaluated both groups). The evaluator blinding method of the remaining six studies was unclear. The integrity of results data in three articles was determined to have a high risk of attrition bias as subjects chose to withdraw from the experiment, however, the remaining articles had a low risk. The presence of reporting bias was determined as unclear in three articles, and low risk in the remaining articles. These results are visualized in Figs 2 and 3.
The authors’ judgments on each risk-of-bias item, presented as percentages across all included studies.
The author’s judgments on each risk of bias item for each included study.
Meta-analysis results
Effect of WBV training on GMFM88-D in children with cerebral palsy.
Seven of the included studies investigated the effect of WBV training on GMFM88-D indices in children with cerebral palsy. The results showed that, in comparison to the control group, WBV training could improve GMFM88-D in these children [WMD = 2.46, 95% CI (1.26, 3.67), Z = 4.01, P<0.01] (Fig 4). Egger’s test showed no publication bias in these seven articles (P = 0.664>0.1). Further analysis showed that heterogeneity was not significant (P = 0.20, I2 = 30%<50%). This leads us to conclude that WBV training combined with conventional physiotherapy could improve the lower limb gross motor function of children with cerebral palsy better than conventional physiotherapy alone.
Effect of WBV training on GMFM88-E in children with cerebral palsy.
Seven of the included studies investigated the effect of WBV training on GMFM88-E indices in children with cerebral palsy. The results showed that, compared with the control group, WBV training could improve GMFM88-E these children [WMD = 3.44, 95% CI (1.21, 5.68), Z = 3.01, P = 0.003<0.01] (Fig 5). Egger’s test showed no publication bias in these seven articles (P = 0.780>0.1) and heterogeneity was non-significant (P = 0.35, I2 = 11%<50%). In summary, WBV training combined with conventional physiotherapy could improve the lower limb gross motor function of children with cerebral palsy better than conventional physiotherapy alone.
Effect of WBV training on 6MWT in children with cerebral palsy.
Four studies investigated the effect of WBV training on 6MWT indices in children with cerebral palsy. Analysis of these studies revealed significant heterogeneity (P<0.01, I2 = 89%). Sensitivity analysis was performed to determine the source of heterogeneity, however, we were unable to eliminate heterogeneity by excluding each article in turn. Thus, the random effect model was selected for analysis. The results showed that, compared with the control group, 6MWT scores were not improved by WBV training (Fig 6). Egger’s test revealed no publication bias in the literature (P = 0.554>0.1).
Effect of WBV training on TUG in children with cerebral palsy.
Four studies investigated the effect of WBV training on TUG indices in children with cerebral palsy. The results showed that, compared with the control group, WBV training could reduce TUG time and risk of falls in these children [WMD = -3.17, 95% CI (-5.11, -1.24), Z = 3.22, P = 0.001] (Fig 7). Egger’s test indicated no publication bias in these four articles (P = 0.436>0.1) and heterogeneity was not significant (P = 0.55, I2 = 0.0%<50%). Thus, WBV training combined with conventional physiotherapy could improve TUG performance of children with cerebral palsy more effectively than conventional physiotherapy alone.
Effect of WBV training on BBS in children with cerebral palsy.
For BBS, three studies investigated the effect of WBV training on BBS indices in children with cerebral palsy. Heterogeneity was significant (P = 0.00, I2 = 96.0%). In order to further understand the source of heterogeneity, sensitivity analysis showed that the heterogeneity decreased significantly after excluding Cai’s (2018) literature (P = 0.49, I2 = 0.0%). The results showed that compared with the control group (S1 Fig), WBV training could significantly improve the balance ability of children with cerebral palsy [WMD = 4.00, 95% CI (3.29, 4.71), Z = 11.01, P<0.01]. In Begg’s test, P = 0.317>0.1 indicated that there was no publication bias in the literature. In conclusion, WBV training combined with conventional physiotherapy was effective on improving the BBS balance ability of children with cerebral palsy than conventional physiotherapy alone.
Effect of WBV training on Ankle function of children with cerebral palsy.
For ankle function, four studies investigated the effect of WBV training on ankle function indices in children with cerebral palsy. Two pieces of literature evaluated the active ROM of the ankle joint in children with cerebral palsy (P = 0.01, I2 = 84%), and the result showed that there was a non-significant difference comparing with the control group (S2 Fig). The results of the passive ROM of the ankle joint in children with cerebral palsy [WMD = 3.78, 95% CI (0.74, 6.81), Z = 2.44, P = 0.01] showed that there were significant differences between the two groups (S3 Fig).
Two pieces of literature evaluated the ankle-R1 [WMD = 5.37, 95% CI (3.24, 7.50), Z = 4.94, P<0.01] and ankle-R2 [WMD = 6.12, 95% CI (4.02, 8.21), Z = 5.72, P<0.01] of children with cerebral palsy. The results showed that there was a significant difference between the two groups, with the experimental group being significantly higher than the control group (S4 and S5 Figs).
In Begg’s test, P = 0.317>0.1, which indicated that there was no publication bias in the literature. In summary, the results showed that WBV training could effectively improve the passive range of motion of the ankle joint and the angle of the ankle joint during muscle reaction in children with cerebral palsy.
Publication bias assessment
The GMFM88-D and GMFM88-E were used as indicators to plot the inverted funnel diagram, using WMD as the abscissa and SE as the ordinate, as shown in Fig 8. It can be seen from the figures that the graphic distribution of the two funnel charts was basically symmetrical, and the scattered points of each study were also within the scope of the inverted funnel chart. The possibility of literature bias was small, and the analysis results were reliable.
Discussion
The incidence of cerebral palsy is gradually increasing with an increasingly younger age of onset and approximately 80% disability in survivors [3, 34]. Most patients with cerebral palsy have motor dysfunction due to brain injury or lesions, which affects the lower limb motor function of patients with cerebral palsy [1–3, 34]. Lower limb rehabilitation in children with cerebral palsy is a clinical difficulty. Although there have been a variety of therapies to improve lower limb function, there is a lack of specific means [35]. A single routine rehabilitation therapy process can be monotonous and the content is boring, the lack of interaction between children and therapists can easily lead to a reduction in the children’s interest, and the heavy workload can also lead to therapists fatigue [36]. Whole-body vibration training is to promote the recovery of limb and joint functions and enhance muscle strength and limb coordination and flexibility through a warm-up, traction, strength training, muscle relaxation and joint injury rehabilitation [37, 38]. Under certain vibration conditions, WBV training has benefits for some people with cerebral palsy, such as reducing spasticity, improving muscle strength, increasing joint mobility and muscle thickness, promoting postural stability, improving balance ability, and enhancing gross motor ability [39]. Moreover, the greatest feature of WBV training is that it can achieve effective rehabilitation with a small load, without causing excessive burdens on the heart and lung, and with little impact on important organs such as the cardiovascular and nervous system [40]. For CP patients, WBV training is simple, non-invasive, relatively safe, and has a short training time. Even one-time intervention can also produce positive effects, which can better stimulate the interest and enthusiasm for rehabilitation in children. The combination of WBV training and conventional treatment may play a better role in rehabilitation potential, thus achieving better treatment outcomes [41, 42].
Although many scholars have used WBV training to improve the lower limb motor function of children with cerebral palsy and most of them have achieved satisfactory results [43, 44]. However, Nordlund (2007), Ruck (2010) and Pozo Cruz (2012) showed that WBV training is not completely effective in improving muscle and nerve function, and the efficacy of treatment remains to be determined [45–47]. In the literature search, the research group found that many RCTs combined with other therapies could not be meta-analyzed and were therefore excluded. Some of the high-quality papers differed in their evaluation metrics and could not be combined and analyzed on the data. In addition, in previous studies on a systematic review of WBV training in children with cerebral palsy, only electromyographic indicators were mentioned, and no other indicators were mentioned by Pozo Cruz (2012) [47]. Therefore, the research group integrative selected GMFM88-D/E score, 6MWT, TUG, BBS and Ankle function as the indexes to evaluate the lower limb motor function of children with cerebral palsy. The analysis results show that:
- WBV training effectively improved the gross motor function of lower limbs in children with cerebral palsy.
- WBV training did not significantly improve the 6MWT walking speed of children with cerebral palsy.
- WBV training effectively improved the TUG performance of children with cerebral palsy.
- WBV training effectively improved the balance ability of children with cerebral palsy.
- WBV training can effectively improve the ankle function of children with cerebral palsy.
In terms of gross motor function, children with cerebral palsy have movement retardation and muscle stiffness in the early stage. Rehabilitation treatment through whole-body vibration training can effectively improve muscle strength and posture control and, in addition, in enhancing the standing ability of patients to walk, run, and jump. This result consistent with previous studies [8], which indicate that the whole-body vibration training has a significant positive impact on the gross motor function of lower limbs.
In terms of 6MWT walking speed, the included literature generally showed no significant difference and great heterogeneity, which means WBV training did not significantly improve the 6MWT walking speed of children with cerebral palsy. However, two of the literatures showed that WBV training was effective and two literatures showed that WBV training was ineffective, which was found by comparison, indicating that the experimental sample size and treatment period of literatures that WBV training was effective were larger than literatures that showed that WBV training was ineffective. Through the analysis of the included original articles, we found that the two articles did not combine conventional training and WBV as treatment methods, and different treatment plans may have different results. In Ahmadizadeh (2019), after the intervention of WBV training, the 6MWT performance of the experimental group was not higher than the control group. The reason may be that, although the results showed that WBV training could improve the muscle strength and coordination, balance and walking speed of children with CP, However, WBV training did not significantly increase the range of motion of knee extension and the passive range of motion of hip flexion, abduction and ankle extension. The experiment also showed that the combination of stretching and WBV did not change the severity of knee muscle spasm in CP children, which may have resulted in no statistically significant difference in 6MWT performance between the experimental group and the control group. Additionally, in Jung (2020), the 6MWT performance increased between the two groups, but the change was not obvious. The reason may be that the control group used WBV training, and the experimental group added action observation. Participants were instructed to watch a video on a 17-inch laptop screen from a distance of 50 cm. During this time, they were instructed to either follow or to not follow the actions demonstrated in the video. However, due to the problems of the experimental group, such as the short attention span of action observation and the unqualified action requirements, the changes of the two groups may not be obvious. Moreover, short intervention time, small study sample size, limited application frequency of WBV, weak control of other factors and other problems, which may also lead to WBV training did not significantly improve 6MWT performance. Cheng (2015) also explained that the improvement in 6MWT was significant, but it gradually disappeared after the intervention stopped [48]. Thus, long-term intervention may be required to achieve more sustained improvements. The differences in the experimental sample size, number of cycles, choice of treatment regimen as well as the measures in RCTs may affect the overall stability, therefore, more experimental studies are needed to verify the effectiveness of WBV training on 6MWT walking speed in children with cerebral palsy.
In terms of TUG performance, the indicators included in the literature indicate that WBV training can effectively improve the TUG performance of children with cerebral palsy, possibly because WBV training enhances the coordination and flexibility of lower limbs, reduces the risk of falls and shortens the testing time of children with cerebral palsy, which is consistent with previous studies [49].
In terms of balance ability, the included literatures differed significantly with large heterogeneity, and after sensitivity analysis, the heterogeneity decreased. In addition, the results of the two groups were also statistically different. Therefore, WBV training can effectively improve the balance ability of children with cerebral palsy. Balance training with different vibration modes and methods, multiple functional activities require patients to actively transfer their center of gravity to maintain dynamic or static balance, which is consistent with previous studies [39, 50], indicating that WBV training can improve patients’ lower limb weight-bearing, balance and walking ability.
In terms of ankle function, WBV training could significantly improve the passive range of motion and ankle angle of the ankle joint during muscle reaction in children with cerebral palsy, but there was no significant difference in the active range of motion of the ankle joint, the reason may be that the differences in the age, sample size, and treatment period of the subjects selected in the two articles resulted in variations in the results Therefore, more experimental studies are needed to verify the effectiveness of WBV training on the active range of motion of the ankle in children with cerebral palsy. On the whole, whole-body vibration training still improved the ankle function of children with cerebral palsy, which is consistent with previous studies [41].
Limitation
This study only includes the published randomized controlled studies and does not include the review and conference literature, which may have a certain impact on the results. Future studies can add inclusion criteria on this basis. Moreover, the research quality of the literature included in this paper is not high. It is suggested that the clinical trial design should be stricter to improve the quality of the research.
The overall sample size of this study is small. The difference between the intervention group and the control group and the intervention cycle may be one of the main reasons for the statistical deviation. It is generally believed that the longer the experimental cycle, the more obvious the therapeutic effect. There are 8 literature whose experimental period is less than 10 weeks, which may affect the overall combined analysis. Therefore, it is suggested that the duration of intervention measures in future research should be 10 weeks as a reference.
At present, the clinical trials of WBV training on the rehabilitation of lower limb motor function are complex and diverse, so that the existing clinical evidence is difficult to meet the actual needs, and the accuracy of the conclusion is significantly reduced. There are few included studies on BBS and Ankle function. In the future, relevant research can appropriately increase and refine the discussion and research of these two indicators. In addition, there is no unified standard for the optimal value of vibration mode, amplitude and frequency in WBV training, which is also a direction for future research.
Conclusion
In conclusion, the analysis results show that WBV training combined with conventional physiotherapy can improve the lower limb motor function of children with cerebral palsy more than conventional physiotherapy alone. This study followed the results of evidence-based medical research and used meta-analysis to combine the results of clinical RCTs on the effects of WBV training on lower limb motor function in children with cerebral palsy. This article overcomes the shortcomings of small experimental samples and incomplete consistency of results and improves the statistical test efficacy. It provides more reliable evidence for clinical practice and decision making of WBV training rehabilitation for children with cerebral palsy.
Supporting information
S1 Fig. Effect of WBV training on BBS balance ability of children with cerebral palsy.
https://doi.org/10.1371/journal.pone.0282604.s003
(TIF)
S2 Fig. Effect of WBV training on Ankle-active ROM in children with cerebral palsy.
https://doi.org/10.1371/journal.pone.0282604.s004
(TIF)
S3 Fig. Effect of WBV training on Ankle-passive ROM in children with cerebral palsy.
https://doi.org/10.1371/journal.pone.0282604.s005
(TIF)
S4 Fig. Effect of WBV training on Ankle-R1 in children with cerebral palsy.
https://doi.org/10.1371/journal.pone.0282604.s006
(TIF)
S5 Fig. Effect of WBV training on Ankle-R2 in children with cerebral palsy.
https://doi.org/10.1371/journal.pone.0282604.s007
(TIF)
Acknowledgments
This work was supported by the Gdansk University of Physical Education and Sport. The authors thank Dr. Cheng for her in-depth discussion on the effect of WBV training on lower limb motor function in children with cerebral palsy.
References
- 1. Patel DR, Neelakantan M, Pandher K, Merrick J. Cerebral palsy in children: a clinical overview. Transl Pediatr. 2020;9(Suppl 1):S125–s35. Epub 2020/03/25. pmid:32206590
- 2. Koman LA, Smith BP, Shilt JS. Cerebral palsy. Lancet. 2004;363(9421):1619–31. Epub 2004/05/18. pmid:15145637
- 3. Graham HK, Rosenbaum P, Paneth N, Dan B, Lin JP, Damiano DL, et al. Cerebral palsy. Nat Rev Dis Primers. 2016;2:15082. Epub 2016/05/18. pmid:27188686
- 4. Qiu A, Yang Z, Li Z. Recent perspectives of cerebral palsy in children. Minerva Pediatr. 2019;71(3):297–303. Epub 2017/03/30. pmid:28353322
- 5. Maeda N, Urabe Y, Sasadai J, Miyamoto A, Murakami M, Kato J. Effect of Whole-Body-Vibration Training on Trunk-Muscle Strength and Physical Performance in Healthy Adults: Preliminary Results of a Randomized Controlled Trial. J Sport Rehabil. 2016;25(4):357–63. Epub 2016/09/17. pmid:27632856
- 6. Stania M, et al. The application of whole-body vibration in physiotherapy—A narrative review. Physiol Int, 2016;103(2): p. 133–145. pmid:28639859
- 7. Alam MM, Khan AA, Farooq M. Effect of whole-body vibration on neuromuscular performance: A literature review. Work. 2018;59(4):571–83. Epub 2018/05/08. pmid:29733043
- 8. Duquette SA, Guiliano AM, Starmer DJ. Whole body vibration and cerebral palsy: a systematic review. J Can Chiropr Assoc. 2015 Sep;59(3):245–52. pmid:26500358
- 9. Song S, Lee K, Jung S, Park S, Cho H, Lee G. Effect of Horizontal Whole-Body Vibration Training on Trunk and Lower-Extremity Muscle Tone and Activation, Balance, and Gait in a Child with Cerebral Palsy. Am J Case Rep. 2018 Oct 31;19:1292–1300. pmid:30377290
- 10. Jung Y, Chung EJ, Chun HL, Lee BH. Effects of whole-body vibration combined with action observation on gross motor function, balance, and gait in children with spastic cerebral palsy: a preliminary study. J Exerc Rehabil. 2020;16(3):249–57. Epub 2020/07/30. pmid:32724782
- 11. Meng WB, Liu FW, Dong C, Yang B, Ma DD, Wang MM, et al. Effects of whole body vibration training on lower limb motor function in children aged 1–3 years with spastic cerebral palsy. Journal of Zhengzhou University (Medical Sciences), 2017;52(06): 740–745.
- 12. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann T, Mulrow CD, et al. Mapping of reporting guidance for systematic reviews and meta-analyses generated a comprehensive item bank for future reporting guidelines. J Clin Epidemiol. 2020;118:60–8. Epub 2019/11/20. pmid:31740319
- 13. Hielkema T, Hamer EG, Ebbers-Dekkers I, Dirks T, Maathuis CG, Reinders-Messelink HA, et al. GMFM in infancy: age-specific limitations and adaptations. Pediatr Phys Ther. 2013;25(2):168–76; discussion 77. Epub 2013/04/02. pmid:23542195
- 14. Ko J, Kim M. Reliability and responsiveness of the gross motor function measure-88 in children with cerebral palsy. Phys Ther. 2013;93(3):393–400. Epub 2012/11/10. pmid:23139425
- 15. Ko J. Sensitivity to functional improvements of GMFM-88, GMFM-66, and PEDI mobility scores in young children with cerebral palsy. Percept Mot Skills. 2014;119(1):305–19. Epub 2014/08/26. pmid:25153757
- 16. Hoffman RM, Corr BB, Stuberg WA, Arpin DJ, Kurz MJ. Changes in lower extremity strength may be related to the walking speed improvements in children with cerebral palsy after gait training. Res Dev Disabil. 2018;73:14–20. Epub 2017/12/16. pmid:29245044
- 17. Parent A, Raison M, Pouliot-Laforte A, Marois P, Maltais DB, Ballaz L. Impact of a short walking exercise on gait kinematics in children with cerebral palsy who walk in a crouch gait. Clin Biomech (Bristol, Avon). 2016;34:18–21. Epub 2016/04/04. pmid:27038653
- 18. Viteckova S, Cejka V, Dusek P, Krupicka R, Kutilek P, Szabo Z, et al. Extended Timed Up & Go test: Is walking forward and returning back to the chair equivalent gait? J Biomech. 2019;89:110–4. Epub 2019/04/16. pmid:30982536
- 19. Nygard H, Matre K, Fevang JM. Evaluation of Timed Up and Go Test as a tool to measure postoperative function and prediction of one year walking ability for patients with hip fracture. Clin Rehabil. 2016;30(5):472–80. Epub 2015/06/26. pmid:26109590
- 20. Hohtari-Kivimäki U, Salminen M, Vahlberg T, Kivelä SL. Short Berg Balance Scale—correlation to static and dynamic balance and applicability among the aged. Aging Clin Exp Res. 2012;24(1):42–6. Epub 2012/05/31. pmid:22643304
- 21. Telenius EW, Engedal K, Bergland A. Inter-rater reliability of the Berg Balance Scale, 30 s chair stand test and 6 m walking test, and construct validity of the Berg Balance Scale in nursing home residents with mild-to-moderate dementia. BMJ Open. 2015;5(9):e008321. Epub 2015/09/09. pmid:26346874
- 22. Dill KE, Begalle RL, Frank BS, Zinder SM, Padua DA. Altered knee and ankle kinematics during squatting in those with limited weight-bearing-lunge ankle-dorsiflexion range of motion. J Athl Train. 2014;49(6):723–32. Epub 2014/08/22. pmid:25144599
- 23. Yan SZ, Jin J, Chen SD, Zhang C, Yu B. Effect of whole body vibration on gait speed and gross motor function of pediatric patients with spastic cerebral palsy: A study of 20 cases. Chinese Journal of Practical Pediatrics, 2021;36(01):33–37.
- 24. Ren XS, Cai ZJ, Zhang XA, Liu J, Chen Z, Zhu DN. Whole body vibration combined with botulinum neurotoxin A injection in the treatment of spastic diplegic cerebral palsy. Chin J Phys Med Rehabil, 2019;41(09):688–692.
- 25. Cai WL, He QY, Chen XF, Zeng XL, Zhang XF. Effect of whole body vibration therapy on gross motor function and balance function in spastic diplegia. Chinese Manipulation & Rehabilitation Medicine, 2018;9(15):8–9.
- 26. Lee W, Lee HS, Park S, Yoo J-K editors. Effects of Whole Body Vibration Training on Lower Limb Muscle Thickness and Gross Motor Function in Children with Spastic Cerebral Palsy. 2019;14(4): 195–201.
- 27. Yin HW, Li HF, Zhang X, Wang H, Ruan WC, Du Y, et al. The effects of whole-body vibration therapy on the lower extremity motor function of children with spastic diplegia. Chin J Phys Med Rehabil, 2019;41(10):752–753-754-755-756.
- 28. Tekin F, Kavlak E. Short and Long-Term Effects of Whole-Body Vibration on Spasticity and Motor Performance in Children With Hemiparetic Cerebral Palsy. Percept Mot Skills. 2021;128(3):1107–29. Epub 2021/02/05. pmid:33535899
- 29. Ibrahim MM, Eid MA, Moawd SA. Effect of whole-body vibration on muscle strength, spasticity, and motor performance in spastic diplegic cerebral palsy children. Egyptian Journal of Medical Human Genetics. 2014;15(2):173–9.
- 30. Ko M-s Doo J-H, Kim J-s Jeon H-S. Effect of whole body vibration training on gait function and activities of daily living in children with cerebral palsy. International journal of therapy and rehabilitation. 2015;22(7):321–8.
- 31. Dudonieo V, Lendraitieo E, Pozeriene J. Effect of vibration in the treatment of children with spastic diplegic cerebral palsy. Journal of Vibroengineering. 2017;19(7):5520–6.
- 32. Ahmadizadeh Z, Amozade Khalili M, Simin Ghalam M, Mokhlesin M. Effect of Whole Body Vibration with Stretching Exercise on Active and Passive Range of Motion in Lower Extremities in Children with Cerebral Palsy: A Randomized Clinical Trial. Iranian Journal of Pediatrics. 2019;29(5).
- 33. Hegazy RG, Abdel-aziem AA, El Hadidy EI, Ali YM. Effects of whole-body vibration on quadriceps and hamstring muscle strength, endurance, and power in children with hemiparetic cerebral palsy: a randomized controlled study. Bulletin of Faculty of Physical Therapy. 2021;26(1):1–10.
- 34. Vitrikas K, Dalton H, Breish D. Cerebral Palsy: An Overview. Am Fam Physician. 2020;101(4):213–20. Epub 2020/02/14. pmid:32053326
- 35. Sajan JE, John JA, Grace P, Sabu SS, Tharion G. Wii-based interactive video games as a supplement to conventional therapy for rehabilitation of children with cerebral palsy: A pilot, randomized controlled trial. Dev Neurorehabil. 2017 Aug;20(6):361–367. pmid:27846366
- 36. Ead H. Change Fatigue in Health Care Professionals—An Issue of Workload or Human Factors Engineering? J Perianesth Nurs. 2015;30(6):504–15. Epub 2015/11/26. pmid:26596386
- 37. Donahue RB, Vingren JL, Duplanty AA, Levitt DE, Luk HY, Kraemer WJ. Acute Effect of Whole-Body Vibration Warm-up on Footspeed Quickness. J Strength Cond Res. 2016;30(8):2286–91. Epub 2016/06/22. pmid:27328378
- 38. Mikami Y, Amano J, Kawamura M, Nobiro M, Kamijyo Y, Kawae T, et al. Whole-body vibration enhances effectiveness of "locomotion training" evaluated in healthy young adult women. J Phys Ther Sci. 2019;31(11):895–900. Epub 2019/12/25. pmid:31871373
- 39. Li GF, Cong Y, Zhou DW, Fang X, Fan YB. Application of whole body vibration stimulation in clinical rehabilitation of cerebral palsy patients. Chin J Phys Med Rehabil, 2016;38(05):397–400.
- 40. Muir J, Kiel DP, Rubin CT. Safety and severity of accelerations delivered from whole body vibration exercise devices to standing adults. J Sci Med Sport. 2013 Nov;16(6):526–31. pmid:23453990
- 41. Yang DH, Wu XP. Intervention Effectiveness of Whole Body Vibration Training on Patients with Cerebral Palsy. Journal of Shanghai University of Sport, 2018;42(02):100–108.
- 42. Bu SM, Han TW. Application of Whole Body Vibration Training in Sports Training and Rehabilitation and Its Research Progress. Journal of Beijing Sport University, 2014;37(08):65–70.
- 43. Cheng HY, Ju YY, Chen CL, Chuang LL, Cheng CH. Effects of whole body vibration on spasticity and lower extremity function in children with cerebral palsy. Hum Mov Sci. 2015;39:65–72. Epub 2014/12/03. pmid:25461434
- 44. Yabumoto T, Shin S, Watanabe T, Watanabe Y, Naka T, Oguri K, et al. Whole-body vibration training improves the walking ability of a moderately impaired child with cerebral palsy: a case study. J Phys Ther Sci. 2015;27(9):3023–5. Epub 2015/10/28. pmid:26504349
- 45. Nordlund MM, Thorstensson A. Strength training effects of whole body vibration? Scandinavian Journal of Medicine & Science in Sports. 2007;17(1):12–17. pmid:17038159
- 46. Ruck J, Chabot G, Rauch F. Vibration treatment in cerebral palsy: A randomized controlled pilot study. J Musculoskelet Neuronal Interact. 2010;10(1):77–83. pmid:20190383
- 47. del Pozo-Cruz B, Adsuar JC, Parraca JA, del Pozo-Cruz J, Olivares PR, Gusi N. Using whole-body vibration training in patients affected with common neurological diseases: a systematic literature review. J Altern Complement Med. 2012;18(1):29–41. Epub 2012/01/12. pmid:22233167
- 48. Cheng HY, Yu YC, Wong AM, Tsai YS, Ju YY. Effects of an eight-week whole body vibration on lower extremity muscle tone and function in children with cerebral palsy. Res Dev Disabil. 2015;38:256–61. Epub 2015/01/13. pmid:25575288
- 49. Saquetto M, Carvalho V, Silva C, Conceição C, Gomes-Neto M. The effects of whole body vibration on mobility and balance in children with cerebral palsy: a systematic review with meta-analysis. J Musculoskelet Neuronal Interact. 2015 Jun;15(2):137–44. pmid:26032205
- 50. Rauch F. Vibration therapy. Dev Med Child Neurol. 2009 Oct;51 Suppl 4:166–8. pmid:19740225