Effect of virtual reality on motor coordination in children with cerebral palsy: a systematic review and meta-analysis of randomized controlled trials

Abstract

Background

Improving motor coordination is an important prerequisite for the functional development of children with cerebral palsy (CP). Virtual reality (VR) may be efficient, interactive, adjustable and motivating physiotherapy choice for children with deficient coordination. This review aimed to identify, evaluate and formulate all the evidence concerning the efficacy of VR on motor coordination in children with CP and to compare the Physiotherapy Evidence Database (PEDro) with Cochrane Risk of Bias (RoB).

Main text

Five databases (PubMed, Cochrane Central Register of Controlled Trials, Web of Science, Science Direct and google scholar) were systemically searched from inception up to 1st January 2019. Studies included VR intervention for children with cerebral palsy with motor incoordination. Studies methodological quality was assessed by Cochrane RoB and PEDro scale. Nineteen studies met the prespecified eligibility criteria. There was a large effect size (SMD 0.75) on fine motor coordination. However, there was a non-significant, small beneficial effect (SMD 0.15) on gross motor coordination. The association between the overall Cochrane RoB and PEDro scores was fair (r = 0.28, P value 0.248). There was a slight agreement between overall and moderate categories PEDro scores and Cochrane RoB (κ = 0.02) and κ = 0.10), respectively. However, high and low categories were moderately agreed with Cochrane RoB (κ = 0.43) and (κ = 0.46).

Conclusion

VR seems to be effective for improving fine motor coordination with questionable effect on gross motor coordination. PEDro scale is fairly correlated with Cochrane RoB, so development and validation of a more compatible quality assessment tools specific to physiotherapy trials are needed.

Background

Cerebral palsy (CP) is characterized by damage of the neonatal or infantile brain which affects the motor system and as a result, the child has poor coordination, poor balance or abnormal movement patterns or a combination of these characteristics [1].

Coordination is defined as the ability of the body to integrate the action of the muscles of the body to accomplish a specific movement or a series of movements in the most efficient manner [2]. Motor coordination is normally classified into two major categories, gross motor and fine motor [3]. Gross motor coordination refers to motor behaviors related to posture and locomotion, from early developmental milestones to finely tuned balance. Fine motor coordination involves motor behavior such as discrete finger movement, manipulations and eye-hand coordination [4]. An important term—dexterity—is often associated with motor coordination which is defined as the manual skill requiring rapid coordination of fine and gross movements [5, 6]. Two main types of dexterity exist: manual and finger dexterities [6]. Both gross and fine motor coordination are essential for performing functional tasks with the upper extremities (UEs) to succeed in daily activities and participate in school, leisure and social activities [7,8,9]. Gross motor coordination provides a stable postural base needed for the acquisition of both gross and fine motor skills. It is essential for the development of fine manual dexterity [10]. Fine motor coordination is important for the performance of activities of daily living such as eating, drinking, body care and fine object manipulation and of special importance for children in school-age because they spend a large proportion of their day coloring and writing which require a high degree of eye-hand coordination [11,12,13].

Impairment of motor coordination not only impacts the motor domain, but also encounters educational, behavioral and socio-emotional domains of the child development [11, 14]. Lack of gross motor coordination forces additional challenge for the child to cope with peers during team sports so he/she feels less physically competent, frustrated and anxious, loses his interest in participating in team and become less socially interactive [15, 16]. Lack of fine motor coordination restricts the performance of self-care activities and the academic achievement and hence diminishes the child’s ability to develop independent and good quality of life [11, 17].

Over the past decades, new trends have been developed to improve sensory motor learning in children with CP [16,17,18]. One of these is virtual reality (VR) which has grown dramatically and represents a hopeful approach in pediatric rehabilitation [19].

VR is an interactive computer-simulated environment which creates the sense of being present in the real world by generating sensory experiences, which include artificial taste, sight, smell, sound and touch [20]. Virtual environment can be classified into two broad categories; immersive and non-immersive; with the immersive being the one by which the user is fully immersed into an artificially generated world as if he stepped into it, while the non-immersive or low-cost environments, the user becomes in contact with the virtual world “not within” [21].

The objective of this systematic review was to identify, evaluate and formulate the evidence- extracted from randomized controlled trials (RCTs) only-concerning the effectiveness of VR in rehabilitation of motor coordination in children with CP and to determine how far the sum scores of Cochrane RoB and PEDro scales are correlated and the degree of agreement between them.

Main text

Methodology

This systematic review was performed according to principles of Preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines [22].

Search strategy

Five electronic databases were searched systematically and comprehensively from inception to 1st January 2019. They included the following English databases: PubMed, Cochrane database of systematic reviews, Web of Science, Science Direct and google scholar.

Medical subject heading (MeSH) terms and key words are of four groups: “virtual reality,” “coordination,” “cerebral palsy” and “children.”

Study selection

Selection of Selection of the studies to be relevant to our review passed by two stages:

Stage 1 (filtration by title and abstract)

Initially, two independent reviewers screened each title and abstract of the yielded search results to determine their eligibility for inclusion. Studies lack any of the eligibility criteria were instantly excluded. Only abstracts met the inclusion criteria or required full text review to confirm that they met all eligibility criteria (i.e., abstracts carrying information that supposed the study potentially relevant to our review) were kept for full-text review.

Stage 2 (full-text filtration)

Then, full-text of the retained abstracts was retrieved and assessed by both reviewers for adherence to inclusion criteria to select the studies to be finally included in the review. Only full-text randomized controlled trials were included. Study reviews, commentaries or reports were used to identify the original article only, otherwise they were excluded. Whenever full-text manuscript or any further details were not available, a contact with the investigator was made by an e-mail. Any conflict about inclusion of the relevant studies was solved by discussion and a third reviewer was consulted if persisted.

Eligibility criteria

Using a PICOS format for questioning (Population, Intervention, Comparison/control, Outcome and study design), we set the eligibility criteria.

Inclusion criteria

• Studies had to fulfill the following criteria to be included in this systematic review:

• Study design was randomized controlled trial.

• 100% of the participants were pediatric patients diagnosed with any form of cerebral palsy aging from 3 up to 18 years.

• Intervention was virtual reality therapy alone or combined with other intervention or within the setup of any other modality against no, placebo or routine physiotherapy treatment.

• Outcome measure was motor coordination.

Exclusion criteria

Studies were excluded if:

• Many publications of the same study reporting the same results.

• Participants are adults or suffering from any disability rather than cerebral palsy.

• Virtual reality is not the intervention of choice.

• Virtual reality used as an evaluative tool not a therapeutic modality.

• Robots are used as an orthosis only and not as VR component.

• Single session intervention is used.

• Not published in English due to shortage of translation resources.

Assessment of risk of bias and strength of evidence

Two quality assessment tools were used to critically appraise the methodological quality of the selected studies; the Cochrane Risk of Bias (RoB) tool as described in the Cochrane Handbook for Systematic Reviews of Interventions (version 5.1.0) [23] and Physiotherapy Evidence Database (PEDro) scale [24,25,26]. Cochrane RoB tool has seven areas to assess the methodology of RCTs, whereas PEDro is an eleven criteria-based tool forming possible scoring of any study from 0 to 10. After assessing the idividual studies for their methodological quality using Cochrane RoB, they were rated according to the Agency for Healthcare Research and Quality standard of “good,” “fair,” and “poor” quality designations using conversion thresholds [27].

A PEDro score of 7 or greater was considered of ‘high quality,’ studies with a score of 5 or 6 were judged of ‘moderate quality’ and those with a score of 4 or less were deemed of ‘poor quality’ [28,29,30]. Two reviewers (S) and (N) independently rated the studies for quality assessment and then checked the scoring together. Any disagreement was solved by consensus.

Before scoring of the included studies and after studying of the Cochrane RoB tool well, we performed a pilot scoring of a previously published SR to make sure of our accurate use and estimation.

The level of evidence which each study add to the literature was evaluated by modified Sackett scale which adapted to rank studies according to their PEDro scores [31].

Data extraction

The data of the included studies were extracted by one reviewer (N) and checked by a second reviewer (S) using a data extraction form adapted from Cochrane’s guidelines [23]. Then, the extracted data were tabulated, summarized narratively, statistically analyzed for calculating the ES together with the confidence interval and scores of the quality assessment were also reported.Information was collected on the basis of participants’ demographic data (Table 1), studies’ methodology (Table 2) and studies outcomes (Table 3).

Table 1 Participants demographic data

Table 2 Studies methodology

Table 3 Studies outcomes

Participant characteristics included age (mean, SD), gender, participant characteristics, the total sample size and the number of patients in each group. Study design, treatments received for both the experimental and the control groups, dosing (duration, frequency, length, and follow-up), VR equipment and its type (immersive vs non-immersive) were collected as methodological characteristics. Study outcomes include the outcome measures, their classification according to the International Classification of Functioning, Disability and Health (ICF), the results and the quality appraisal scores. Also, the author name and year of publication were reported. Any disagreement was solved by a consensus method.

Categorization of each outcome measure of the selected studies into ICF dimension was based upon a published literature. ICF domains are divided into two clusters (1) body structure and functions; and (2) activities and participation [50]. Activities were separated from participation because we wanted to illuminate whether or not participation outcomes were being examined. Investigators were contacted via emails if important data were unclear or unavailable.

Data synthesis

Estimation of the treatment effect

This meta-analysis combined data at the study level. The outcome variables were fine motor coordination and gross motor coordination. To allow comparison of data from different scales, pooled statistics were calculated using standardized mean differences (SMDs) with 95% confidence intervals (CIs), which were computed using Comprehensive Meta-Analysis program (CMA, version 3.3.070). Means and SDs at the end of the treatment for the treatment and control groups (when relevant) were used to compute SMDs. If appropriate, estimated effect size was calculated if the outcome variable was reported in ≥ 2 studies.

Since all the outcomes were continuous, they were pooled across studies and analyzed using a random-effects model for data collected from all eligible acute studies obtained from review and data collected from all eligible intervention studies obtained from review. A random-effects model was used because it involves the assumption of statistical heterogeneity across studies.

The effect estimate was classified as described by Cohen’s three levels for the size of the between-group effects (i.e., SMD of less than 0.5 was considered to indicate a small beneficial effect, SMD from 0.5 to less than 0.8 medium or SMD ≥ 0.8 carry a large effect) [51].

Unit of analysis

Crossover studies

Crossover studies were included only when outcome data for the first period of intervention were available or could be obtained upon request from the study authors.

Studies with multiple treatment groups:

In case the study had multiple treatment groups, only the data for relevant treatment groups were included to create a single pair-wise comparison.

Assessment of heterogeneity

Heterogeneity was assessed between studies using the I² statistic to quantify the proportion of the total outcome attributed to variability among studies. The following values were used: I² = 0–30% (no heterogeneity); I² = 30–49% (moderate heterogeneity); I² = 50–74% (substantial heterogeneity); and I² = 75–100% (considerable heterogeneity) [52]. The statistical analysis was conducted by using Comprehensive Meta-Analysis program for windows (CMA, version 3.3.070, Biostat, Inc. USA).

Correlation and agreement between study quality assessments with both tools

To examine the degree of association between PEDro which is the best physiotherapy quality assessment tool and Cochrane which is the gold standard medical quality assessment tool, the yielded studies were further classified as adequate quality if generation of random sequence, concealment of allocation and blinding of outcome assessors were emphasized [53]. Because of the nature of the physiotherapy intervention modalities—in most situations can’t not permit complete blinding of therapist and participant—performance bias was not included as a criteria in such judgment. So studies met three, two, one criteria were good, fair and poor quality, respectively. The statistical analysis for correlation between the scores obtained with the RoB and PEDro scales was assessed by using the statistical SPSS Package program version 24 for Windows (SPSS, Inc., Chicago, IL) by the nonparametric Spearman rank correlation coefficient because normal distribution could not be ascertained for all the parameters studied.

Spearman coefficient values were interpreted as an excellent relationship ≥ 0.91; good, 0.90 to 0.71; moderate, 0.70 to 0.51; fair, 0.50 to 0.31; and little or none, ≤ 0.3 [54].

Also, the strength of agreement between the scores of the 2 scales was measured by Cohen k coefficient categorical data (95% CI) for the overall grades and, with k < 0.20 indicates slight agreement; 0.21–0.40 fair agreement; 0.41–0.60 moderate agreement; 0.61–0.80 substantial agreement; and 0.81–1.0 almost perfect agreement [55]. Significance was set at p < 0.05.

Results

Systematic search results

The flow of different search stages and reasons for exclusion were outlined using a PRISMA diagram flow as shown in (Fig. 1). A total of potentially relevant 2347 citations were yielded, 968 from Pubmed, 571 from Web of Science, 105 from the Cochrane Library, 524 from Google Scholar and 179 from Science Direct. The identified citations were exported to Mendeley software which initially removed 383 duplicates. Then, the full-text of 271 citations was retrieved after the screening of the titles and abstracts of the remaining identified citation. Finally, a total of 19 studies were included in our review based upon full-text examination.

Fig. 1

PRISMA flow diagram

Characteristics the included studies

A detailed information about the study populations, study interventions strategy and outcomes measured is shown in Tables 1, 2 and 3.

Studies participants

A total of 645 participants were recruited with a 570 were who continued to the post-intervention assessments. Sample size ranged from 16 to 102 participants. The majority of the recruited participants were males 299 (54.56%) from a total of 548 participants in 15 studies which specify the participants sex with 6 of them removed the withdrawn participant (dropped-out) from the personal characteristics [32, 35, 38, 43, 47, 56], while 3 studies did not specify the gender of the both groups [37, 40, 41]. The mean age was ranging from 7.05 to 11.67 years in the experimental group and from 7.25 to 12.4 in the control group with two study did not report the mean for each group [40, 41]. Participants in seven of the selected trials were hemiplegic [34, 36, 38, 42,43,44,45] with mixed topographical distribution in five [32, 37, 48, 49, 56], diplegic in four [35, 39, 42, 46], whereas three did not clarify the distribution of CP [40, 41, 47]. At least 55.56% (355) of the patients were affected by spastic hemiplegic, 128 (20.03%) with spastic diplegic CP, 10 (1.56%) with spastic quadriplegic, 5 (0.78%) with triplegic forms of CP.

Types of intervention

One of the included studies had a four comparison arms, comparing VR and rehabilitation to constraint-induced movement therapy (CIMT) and rehabilitation to VR, CIMT and rehabilitation to rehabilitation alone [34]. Two groups (VR versus control group (CG)) were selected for inclusion in our review. However, all the other studies had two arms comparing either VR alone or when combined with usual care or VR training with transcranial direct current stimulation to usual care or no intervention or sham transcranial current direct stimulation. In the term of sophostication, fifteen studies utilized the commercially low-cost sets, whereas four used the engineer-built. Participants in fourteen studies received VR as an adjunctive therapy to conventional treatment, whereas others in another three studies received VR alone and in two studies, the participants received VR followed by a period of conventional treatment or no treatment or vice versa utilizing a crossover design. Location of VR therapy varied from laboratory, clinic or home-based. An overview of the characteristics of the eligible studies is presented in Table 2.

Types of outcome measures

A variety of assessment tools were used to evaluate different aspects of neuromotor status (e.g., coordination, strength, muscle tone) and functional performance.

The International Classification of Function (ICF) outlines two main domains of function for assessment: body function and structure domain and activity and participation domain (subdivided into activity subdomain and participation subdomain).

Through the use of ICF classification, we found that the majority of the outcome measures used in the included studies fit within the activity subdomain of the ICF model with lesser extent measures falling under the body function and structure domain while the participation domain having the least number of outcome measures. Table 3 represents different assessment scales used with their ICF classification.

Fine motor coordination

Under the body function and structures lies joint kinematics and Visual Motor integration (VMI) test, whereas Jebsen Taylor Test of Hand Function (JTTHF), Nine-hole Peg test and Peabody Developmental Motor Scale-2 PDMS-2 assess activity. BurininksOsteretsky Test of Motor Proficiency (BOTMP) “subset 8” lies under both categories.

JTTHF was used in three studies, joint kinematics, VMI test, PDMS-2 and Nine-hole Peg test are used once.

Gross motor coordination

Under the body function and structure lies Modified sensory organization test, reactive balance, Static Posturography, joint kinematics, 10 s climbing test (10s CT), standing durations, 3D temporo-spatial and full-body kinematic gait and motor evoked potential analysis, while Pediatric balance scale (PBS), Box and Blocks test (BBT), Rhythmic weight shift, Walking Speed and Distance, 10 min walking test (10m WT),sit-to-stand test(STST), Timed up and Go test, functional reaching tests, Wii Nintendo Fit Balance and Game Scores lie under the activity section of coordination. BOTMP-2 lies under both categories.

PBS was used in five studies, stabilometric evaluation center of pressure (COP) in 4, 3D temporo-spatial and full-body kinematic gait analysis, timed up and go (TUG) in 3, joint kinematics and BBT twice and Modified sensory organization test, reactive balance, Rhythmic weight shift, 10 sCT, STST, standing durations, Walking Speed & Distance, 10 m WT, functional reaching tests, Wii Nintendo Fit Balance & Game Scores and motor evoked potential were used once.

Intervention protocols

Studies used different treatment strategies with different durations from 3 up to 20 weeks, session duration ranging from 15 to 90 min and frequency 2 to 6 sessions/week.

Effect of interventions

Fine motor coordination

Six studies provided post-intervention assessment of fine motor coordination on 255 participants [34, 36, 38, 40, 42, 44]. There was a low certainty level according to Cochrane RoB that VR a large beneficial effect than the controls immediately post-intervention (SMD 0.75, 95% CI 0.02–1.51) (Fig. 2). Between-study heterogeneity was considerable (I² = 86%). On the other hand, when assessed by modified Sackett scale, the overall evidence for fine motor coordination was moderate that VR intervention is better than the control groups (83.3% n = 5 studies were scored as Ib).

Fig. 2

Forest plot of the effect of VR on fine motor coodination in children with CP

Gross motor coordination

Fourteen studies on 363 children with CP were found to carry a low certainty level with respect to Cochrane RoB about the non-significant small beneficial effect on gross motor coordination brought out immediately following VR (SMD 0.15; 95% CI, 0.09 to 0.40) [32, 33, 35,36,37, 39, 41, 43, 45,46,47,48,49, 56] (Fig. 3). On modified Sackett’s scale, 55.04% of studies have a moderate evidence. Between-study heterogeneity was negligible (I² = 24%). Since only 55.04% of the studies carry a moderate evidence, pooling of individual evidence scoring for each study to reach the overall evidence outweighs a limited evidence.

Fig. 3

Forest Plot of the effect of VR on gross motor coordination in children with CP

Correlation of the total scores obtained with both quality scales

There was a non-significant difference between Cochrane RoB and PEDro scores (p value = 0.248) carrying a fair positive correlation (r = 0.28). The degree of overall agreement between the total scores of the two quality scales was slight (κ = 0.02; (95% CI − 0.02 to 0.50) with non-significant difference (p value = 0.433).

High and low PEDro scores revealed moderate agreement with Cochrane RoB (κ = 0.43 (95% CI 0.36–0.49) and 0.46; (95% CI 0.40–0.51)), respectively, with a significant difference (p = 0.0001) for both. However, when compared with Cochrane RoB, moderate quality studies on PEDro exhibited slight agreement with no significant difference (κ = 0.10; (95% CI − 0.09 to 0.29), p = 0.404).

Quality assessment

Figure 4 and Table 4 display a summary of the quality appraisal scores for each study by Cochrane RoB and PEDro, respectively. Scores were heterogeneous depending on the trial and the quality scale used. When assessed by Cochrane risk of bias assessment tools, all the included studies are considered to have a high risk of bias.

Fig. 4

Risk of bias: each risk of bias item presented as percentages across all included studies

Table 4 PEDro scores

Whereas, when assessed by PEDro scale, more than half of the included studies (57.9%, n = 11) were of moderate quality [32, 34, 35, 37, 39, 41, 42, 44,45,46, 48], about the quarter of studies (26.13%, n = 5) of a high quality [36, 38, 43, 47, 49], whereas three studies (15.8%) were of a low quality [33, 40, 56].

Discussion

The objective of this systematic review was to synthesize the state of the evidence about the effect of virtual reality training on motor coordination in children with cerebral palsy. In order to achieve this aim, a list of strict eligibility criteria were set, nineteen RCTs matching the pre-defined inclusion criteria were evaluated for methodology and the reported results being analyzed statically.

This systematic review could not provide a firm conclusion about the superiority of VR therapy over usual care or no intervention for motor coordination in children with CP. The results revealed that there is a moderate evidence when assessed by modified Sackett scale in favor of VR for fine motor coordination. On the other hand, there was a conflicting evidence for gross motor coordination when assessed by modified Sackett scale moderate to limited. Pooled results showed non-significant small effect of VR-based therapy for gross motor coordination.

Although Cochrane RoB and PEdro scales share the same scoring domains (PEDro has 71.4% of Cochrane scale), the quality of the included studies showed a great rating variations upon assessment by both. This variation is mainly due to different and more restrictive judgment criteria of Cochrane risk of bias than PEDro scale. All the included studies were rated as poor quality when assessed by Cochrane risk of bias; which is to a great extent due to incomplete blinding. Because of the nature of treatment using VR, this criteria could not be satisfied. Surprisingly, even if they were assessed again as having an adequate quality on Cochrane on the basis of generation of random sequence, concealment of allocation, and blinding of outcome assessors, the association and overall agreement between PEDro and Cochrane scores were only fair and slight, respectively. However, categorical agreement between PEDro and RoB was only moderate on the extreme categories (high and low) because the precise methods of randomization and concealment and blinding were accidently reported in many studies while the vast majority moderate ranks on PEDro (11 studies) were slightly agreed with RoB ranks which is logic because most of these studies ranked poor on RoB because the actual methods of randomization or concealment were not reported as required by RoB.

The improvement brought out through VR relies mainly on motor learning which requires many elements available in VR. This includes repetitions, feedback and motivation [57]. VR provides an opportunity for trial and error practice which requires a lot of repetitions together with feedback about performance success provided by the senses (e.g., vision, proprioception) can produce an incremental success and structural cortical changes [58]. But to practice movements more and more, participants must be motivated [58]. Unlike traditional exercise programs, VR not only allow repetitive practice but also engage the cognitive functions in problem solving for better motor learning [59]. Also, VR allows training in a real-world-simulated environment for better performance transfer.

The non-significant small treatment effect size of VR gross motor coordination may be attributed to incorporation of the commercially available VR devices which are not designed to be modified to meet the needs for children with physical impairments. Also, use of the immersive type of VR may improve the results as they enhance the sense of being present.

Adverse events

Only seven studies out of the nineteen studies clearly stated that there were no adverse effects of using VR occurred during their studies [32, 36,37,38,39, 48, 49], however, the remaining studies did not report the possible adverse events [33,34,35, 40,41,42,43,44,45,46,47, 56].

Limitations

The findings of this review are limited to non-immersive VR devices. So, we cannot generalize the effect of VR on motor coordination unless more studies including the immersive types of VR are performed. Several limitations of this review have been identified.

Although in-depth literature search was carried out, because resources were limited, we included only studies published in the English language, potentially excluding other important evidence. Four studies were published in a language other than English. However, the possibility of publication bias could not be excluded, as we did not attempt to retrieve unpublished studies. The potential effects of VR training dosage, game selection and case severity on the effectiveness of VR could not be ascertained because of large heterogeneity in reported data.

Research implications

A more rigorous well designed RCTs with larger sample sizes need to be conducted regarding the effect of virtual reality in children with CP impairing motor coordination with investigation of the optimal duration and frequency of virtual reality. Also, the more immersive types of VR should be recruited.

Conclusion

This systematic review yielded a moderate evidence about large effect of virtual reality on fine motor coordination in children with cerebral palsy when compared to other interventions and conflicting evidence that virtual reality could carry larger effect on gross motor coordination in the intervention group than the control group. Nevertheless, virtual reality could be used safely as a supplemental intervention for motivating children engaging in therapy. PEDro scale demonstrated a fair correlation when compared with Cochrane RoB, so development and validation of a more compatible quality assessment tools specific to physical therapy trials are needed.