[go: up one dir, main page]
More Web Proxy on the site http://driver.im/
Next Article in Journal
An Assist-as-Needed Control Strategy Based on a Subjective Intention Decline Model
Next Article in Special Issue
Usage of Virtual Reality Technology in Physiotherapy in Germany: Results from a Survey
Previous Article in Journal
Comparison of Three Internal Fixation Constructs for AO/OTA 33-A3 Distal Femoral Fractures: A Biomechanical Study
You seem to have javascript disabled. Please note that many of the page functionalities won't work as expected without javascript enabled.
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Bioengineering
Volume 11
Issue 11
10.3390/bioengineering11111112
bioengineering-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

Virtual Reality-Based Therapy Can Enhance Balance and Muscular Endurance in Children and Adolescents with Down Syndrome: A Systematic Review with a Meta-Analysis

by
Marina Piñar-Lara
1,2,
Irene Cortés-Pérez
2,*,
Ángeles Díaz-Fernández
2,
María de Alharilla Montilla-Ibáñez
3,
Ana Sedeño-Vidal
2 and
Esteban Obrero-Gaitán
2
1
CAIT APROMPSI, C/Clara Campoamor 8, 23470 Cazorla, Spain
2
Department of Health Sciences, University of Jaén, Campus Las Lagunillas s/n, 23071 Jaén, Spain
3
Otorhinolaryngology Service, University Hospital “City of Jaen”, 23007 Jaen, Spain
*
Author to whom correspondence should be addressed.
Bioengineering 2024, 11(11), 1112; https://doi.org/10.3390/bioengineering11111112
Submission received: 25 September 2024 / Revised: 25 October 2024 / Accepted: 31 October 2024 / Published: 4 November 2024
(This article belongs to the Special Issue Virtual, Augmented and Mixed Reality for Physiotherapy Interventions)
Browse Figures
Figure 1
<p>The PRISMA flow diagram for the study selection process.</p> "> Figure 2
<p>The forest plot of the effectiveness of VRBT in increasing functional balance [<a href="#B69-bioengineering-11-01112" class="html-bibr">69</a>,<a href="#B70-bioengineering-11-01112" class="html-bibr">70</a>,<a href="#B71-bioengineering-11-01112" class="html-bibr">71</a>,<a href="#B72-bioengineering-11-01112" class="html-bibr">72</a>,<a href="#B73-bioengineering-11-01112" class="html-bibr">73</a>,<a href="#B74-bioengineering-11-01112" class="html-bibr">74</a>].</p> "> Figure 3
<p>The forest plot of the effectiveness of VRBT in increasing dynamic balance [<a href="#B69-bioengineering-11-01112" class="html-bibr">69</a>,<a href="#B74-bioengineering-11-01112" class="html-bibr">74</a>,<a href="#B77-bioengineering-11-01112" class="html-bibr">77</a>].</p> "> Figure 4
<p>The forest plot of the effectiveness of VRBT in increasing static balance with open and closed eyes [<a href="#B70-bioengineering-11-01112" class="html-bibr">70</a>,<a href="#B75-bioengineering-11-01112" class="html-bibr">75</a>].</p> "> Figure 5
<p>The forest plot of the effectiveness of VRBT in increasing muscular endurance [<a href="#B69-bioengineering-11-01112" class="html-bibr">69</a>,<a href="#B73-bioengineering-11-01112" class="html-bibr">73</a>,<a href="#B76-bioengineering-11-01112" class="html-bibr">76</a>,<a href="#B77-bioengineering-11-01112" class="html-bibr">77</a>].</p> ">
Versions Notes

Abstract

:
Physical exercises are crucial for enhancing postural balance and muscle strength in children and adolescents with Down syndrome (DS). Virtual reality-based therapy (VRBT), which utilizes exergames, can favor performing physical activity. The aim of this review was to assess the effectiveness of VRBT in improving balance and muscular endurance in children and adolescents with DS. Since inception up to August 2024, we screened in PubMed Medline, SCOPUS, WOS, CINAHL, and PEDro studies that assessed the effectiveness of VRBT, compared to conventional therapy (CT) or usual care (UC), in improving balance and muscular endurance in DS. Methodological quality was assessed using the PEDro scale. Effect size in meta-analyses was calculated with the Cohen’s standardized mean difference (SMD) and its 95% confidence interval (95% CI). Nine studies providing data from 424 participants with good methodological quality (PEDro: 6.3 ± 1.2 points) were included. Our meta-analysis showed that VRBT is more effective than controls in increasing function (SMD = 1.22; 95% CI 0.64 to 1.81; p < 0.001), dynamic balance (SMD = −2.2; 95% CI −3.1 to −1.25; p < 0.001), and muscular endurance (SMD = 1.37; 95% CI 0.58 to 2.2; p < 0.001). This is the first meta-analysis to exclusively focus on children and adolescents with DS, demonstrating the effectiveness of VRBT in enhancing balance and muscular endurance.

1. Introduction

Down syndrome (DS) is the most prevalent genetic neurodevelopmental disorder in children, occurring in approximately 1 in 800 [1] or 1 in 1000–1100 births worldwide [2]. DS is caused by the presence of an extra copy of chromosome 21 (Hsa21; trisomy 21) in somatic cells, resulting from a process known as nondisjunction [3]. Individuals with DS exhibit various motor and mental developmental clinical manifestations [4,5] as well as other conditions such as congenital heart diseases, low physical endurance, sleep disorders, or orofacial impairments [6,7,8]. The most significant motor impairments in DS are related to joints and muscles, characterized by joint laxity due to hypotonia or muscle weakness (resulting from reduced muscle tone), which negatively impacts muscle strength [9,10]. This predisposes individuals with DS to alterations in postural balance in both static and dynamic conditions, hindering coordination and mobility during functional tasks [11]. Additionally, visual and hearing disorders, among others, can contribute to distorted balance in individuals with DS [12]. Several studies have reported that decreased postural balance is correlated with a high risk of falls [13], restricting participation in school and social community activities and reducing quality of life [14]. Currently, more than 200,000 individuals are living with DS [15], and according to the new Global Burden of Disease of DS, the years lived with disability are increasing [16] highlighting the importance of conducting novel interventions that improve motor and balance disorders to reduce disability.
Given the critical role of visual, vestibular, hearing, and proprioceptive inputs in maintaining balance under both static and dynamic conditions [17], it is essential that therapies for these individuals incorporate these stimuli. To date, physiotherapy interventions, such as kinesio taping in feet muscles, classical balance training exercises, muscle strengthening, neuromuscular stretching exercises, and more innovative approaches like dance interventions or dual-task exercises, have demonstrated effectiveness in improving balance in these children [18,19,20,21]. In addition to them, virtual reality (VR) devices are novel technological devices that can be used in the rehabilitation of a wide variety of physical, cognitive, and psychologist pediatric conditions [22,23,24,25]. Virtual reality-based therapy (VRBT) is the use of VR devices for therapeutics purposes. VR is an advanced type of human–computer interface that allows users to immerse themselves in and engage with a highly realistic computer-generated environment, providing visual, auditory, and proprioceptive stimuli [26]. According to the level of immersion and presence offered to users with these VR devices, the most frequent modalities of VR are non-immersive or immersive. Non-immersive VR consists of the visualization of virtual environments in classical and bi-dimensional screens. In these systems, the individual can interact with the virtual environments using a mouse, hand-controller, or joystick [27]. Commercial examples of this technology are Nintendo or Xbox adding Kinect Sensor. Opposite, immersive VR, to date less used in research and clinical practice, favor the visualization of environments in 360° (full immersion) using head-mounted displays [28]. Meta Quest 2 and 3 is one of the most used immersive VR devices in rehabilitation. Exergames are the primary video games utilized in rehabilitation with VR devices. Particularly for children, the motivation derived from playing in these virtual and playful environments enhances participation in therapy, potentially increasing the benefits of VRBT [29]. VR devices enable the simulation and practice (including at home) of various sports, such as tennis, basketball, and football. Moreover, affordable commercial video games that promote repetitive physical exercise tasks tailored to each child’s specific disabilities can aim to activate and reorganize brain areas, catalyzing neuroplasticity changes related to improvements in movement, balance, or other cognitive functions [30,31].
Compared to others, neurodevelopmental disabilities more extensively studied in the literature, such as cerebral palsy [32], the use of exergames as VRBT in children and adolescents is a novel neurorehabilitation intervention that could potentially improve motor and balance impairments as well as physical condition in these individuals [33,34]. Several reviews published between 2015 and 2021 [35,36,37,38,39] have suggested the beneficial effects of VRBT, compared to conventional therapies (CT), in improving motor learning, balance, muscle strength, or aerobic endurance. While these reviews present insightful findings, recent studies published since the last review highlight the need to update the existing literature. To the best of our knowledge and to enhance the generalization of findings, standardizing the study population, including only studies that provide data on children and adolescents, is essential due to the fact that the majority of published research focuses on individuals within these age groups. Therefore, we hypothesize that VRBT could be effective in increasing balance and muscular endurance in this population. Therefore, the aim of our systematic review with a meta-analysis was to retrieve all published evidence to assess the effectiveness of VRBT in improving balance and muscular endurance in children and adolescents with DS. Additionally, we want to evaluate the effect of VRBT according to specific comparison therapies and whether the effect is similar in children or adolescents.

2. Materials and Methods

2.1. Type of Study and Register

To achieve the objective, a systematic review with meta-analysis was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA 2020 version) [40]. Additionally, the Cochrane Handbook for Systematic Reviews of Interventions and The Handbook of Research Synthesis and Meta-analysis were consulted for methodological aspects [41,42]. The quality of this systematic review was assessed using the AMSTAR 2 checklist [43]. Finally, the protocol of this systematic review was previously registered in PROSPERO database (CRD42024542230).

2.2. Literature Search and Databases Consulted

Since inception up to August 2024, two authors (M.P.-L. and I.C.-P.) conducted a literature search in PubMed Medline, SCOPUS, Web of Science (WOS), CINAHL Complete, and PEDro (Physiotherapy Evidence Database), which was supervised by an expert third author (E.O.-G.). Additionally, this search was complemented screening in the reference list of reviews previously published, proceedings, abstracts, and other sources such as Google Scholar that report studies from journals without impact factor. The research question of this review, according to PICOS tool [44], was as follows: Is VRBT more effective than others in increasing postural balance and muscular endurance in children and adolescents with DS? With the aim to retrieve the major quantity of potential studies to be included in the review, our search strategy was designed using the population (DS) and intervention (VRBT) conditions. It allows us to revise more studies, identifying more that meet the inclusion criteria. Therefore, the key terms used in our search strategy, according to MeSH Thesaurus, were “down syndrome”, “virtual reality”, “virtual reality-exposure therapy”, and “exergaming”. Additionally, other entry terms were used. Table 1 shows the search strategy used in each database and the search terms. Boolean operators (“AND” to join conditions, and “OR” to join related terms in each condition) and specific tags for each database were used. Finally, filters related to language, publication date, and free full access were not applied.

2.3. Study Selection: Inclusion and Exclusion Criteria

All studies retrieved with the literature search were revised in detail for two authors independently (M.P.-L. and I.C.-P.). When one author highlighted a study as having potential to be included in the review, it was examined by the two authors. The level of agreement between authors was known when calculating the Cohen’s kappa coefficient (κ) [45] (κ < 0, non-existent; 0 ≤ κ ≤ 0.2, non-significant; 0.2 < κ ≤ 0.4, discrete; 0.4 < κ ≤ 0.6, moderate; 0.6 < κ ≤ 0.8, substantial; and 0.8 < κ ≤ 1, excellent [46]. Finally, a third author (E.O.-G.) was consulted to solve doubts and discrepancies. The main inclusion criteria were established according PICOS tool: (1) population, children, and adolescents with DS; (2) intervention (VRBT); (3) control intervention (conventional therapy or usual care [UC]; (4) outcomes, postural balance, and muscular endurance; and (5) study design, randomized controlled trials [RCTs], pilot RCT or quasi-experimental studies with randomization, and two groups. Other inclusion criteria related to meta-analysis were that studies included must provide statistical data to conduct the meta-analysis. Oppositely, we excluded studies that included adults with DS and studies that compared two groups; one of them comprised healthy controls or studies that mixed participants with DS and other neurological diseases.

2.4. Data Extraction

Two authors (M.P.-L. and A.D.-F.), independently, were in charge of extracting the followings data from the studies included in the review: (1) overall characteristics of the studies: authors’ names, year of publication, setting, funding, type of study, blinding, total sample size, age and sex, and number of groups; (2) information of VRBT: modality of VR devices employed (non-immersive or immersive), VR device and video game used, and protocol of application in VRBT (number of sessions, weeks, sessions per week, and duration of each session); (3) information of control intervention: whether it was CT or UC and its protocol of application; and (4) data about variables of interest: name of each variable, test employed, and mean and standard deviation of the post-intervention assessment. In each case where standard deviation was not provided, it was estimated trough other data, such as interquartile range, standard error, or range, according to standardized and validated procedures [41,47]. Doubts in this stage were consulted with a third author (I.C.-P.).

2.5. Variables

The variables assessed in this systematic review were postural balance (functional, dynamic, and static) and muscular endurance. On the one hand, related to postural balance, functional balance is a postural balance’s dimension that informs the level of balance during functional tasks or activities; dynamic balance is the ability to maintain standing and stable during movements or displacements; and static balance is the ability to maintain the body in a position without displacements or movements [48,49,50]. On the other hand, muscular endurance refers to the capacity of muscles to sustain exercise [51].

2.6. Assessment of the Methodological Quality, Risk of Bias, and Quality of Evidence

The assessment of the methodological quality and the risk of bias in individual studies and quality of evidence of findings in each meta-analysis were performed by two authors independently (M.A.M.-I. and A.S.-V.) and discrepancies were solved by a third author (I.C.-P.).
The PEDro scale was used to assess the methodological quality, which has been recommended to use in physiotherapy RCTs [52]. This scale comprises 11 items that can be scored as yes (adding 1 point if criterion is met) or no (opposite) [53]. The total score obtained for each RCT can range from 0 to 10 by adding points 2 to 11. According to this, the methodological quality of each RCT can be excellent (10-9 points), good (8-6 points), moderate (5-4 points), and low (3-0 points) [54]. Using this scale can help us to identify biases if some criteria are not met. Items 2 and 3 are related to selection bias, items 5 and 6 with performance bias, and item 7 with detection bias.
The quality of evidence of each meta-analysis was estimated in basis of the Grading of Recommendations Assessment, Development, and Evaluation (GRADE) tool [55,56] and from Meader’s GRADE checklist [57]. To establish the quality or level of evidence, the items taken into account are risk of bias in individual studies, inconsistency (or heterogeneity), imprecision, and indirect evidence. The quality of evidence will be downgraded for each item not met and risk of publication bias. The quality of evidence can be strong (all items are met and results are consistent), moderate (one item is not met, and new studies can change the result of the meta-analysis), low (indicates instability of the findings), and very low (findings can be taken into account with a lot of caution).

2.7. Statistical Analysis

The statistical software Comprehensive Meta-Analysis version 4 (Biostat, Englewood, NY, USA) was used to perform the meta-analysis [58]. Meta-analyses and subgroup analyses only were conducted if at least 2 studies provided data for it [41]. The pooled effect size was calculated with the Cohen’s standardized mean difference (SMD) and its 95% confidence interval (95% CI) in a random-effects model for continuous data [59,60] graphically displayed in forest plots [61]. Pooled effect size was interpreted according Kinney et al. (2020), who suggested that the effect size in rehabilitation studies could be null (SMD 0), small (SMD 0.08–0.15), medium (SMD 0.19–0.36), and big (SMD > 0.4) [62]. When it was possible, as an additional analysis, we estimated the mean difference as effect result to compare it with the minimum clinically important difference (MCID) in outcomes assessed with the same measurement [63]. The literature suggests that to compare the mean difference with the MID value for a measurement test, the most important optimal method is used to assess the clinical relevance or importance of a result [64]. Risk of publication bias was assessed with the funnel plot, with the p-value for Egger test, and with the trim-and-fill method. Heterogeneity (inconsistency) was estimated with the chi-square test and its p-value (p < 0.05 confirms heterogeneity) and the degree of inconsistency of Higgins (I2) [65]. Heterogeneity can be null (I2 0%), low (I2 10–25%), medium (I2 25–50%), or large (I2 > 50%) [66].

2.8. Secondary Analyses

As secondary statistical analysis, we conducted the following. First, a sensitivity analysis using the leave-one-out method (one study removed method) was performed with the aim to assess the contribution of each study in the global pooled effect size. Later, we conducted two subgroup analyses to assess the possible differences between the effect of VRBT according to the comparison intervention (VRBT vs. CT and VRBT vs. UC) and in function of the age group of the participants (children and adolescents). To assess if differences were statistically significant between group, a meta-regression was carried out.

3. Results

3.1. Study Selection

The literature search retrieved 217 studies (212 from the five databases consulted and 5 from other sources). After removing duplicates, 163 were screened by title and abstract, of which 146 were excluded for not being relevant and 6 for not meeting the inclusion criteria. Two studies, although they met the inclusion criteria and were included in previous reviews, were excluded for providing data on adult individuals with DS [67,68]. Finally, nine studies were included in the present systematic review with a meta-analysis [69,70,71,72,73,74,75,76,77] (Figure 1). In the study selection process, an excellent level of agreement between authors was reported (κ = 0.89).

3.2. Characteristics of the Studies Included

The included RCTs, conducted in Taiwan [76], Indonesia [74], Saudi Arabia [69], Pakistan [70], Egypt [71], Brazil [72], Spain [77], and Chile [75] between 2010 and 2024, provided data from 424 individuals with DS (56% boys) with a mean age of 10.9 ± 3.1 years old. The inclusion criteria about the level of intellectual disability in the participants should allow us at least to understand the instructions of video games (mild–moderate intellectual disability). The intervention group who carried our VRBT comprised 188 participants (mean age of 10.7 ± 3.2 years old). Non-immersive VR devices were used as VRBT in eight RCTs [69,70,71,72,73,75,76,77] (Nintendo Wii video games being the most employed), and only one used immersive VR [74]. VRBT was used as unique therapy in all studies except for the study of Rahman et al., 2010, that was applied in combination with CT exercises [71]. The protocol application of VRBT in the included RCTs ranged from 8 to 60 sessions received during a period of 4 to 24 weeks between two and six sessions per week and between 20 and 60 min of VRBT exposition in each session. The control group comprised 236 participants (mean age of 10.6 ± 2.9 years old) received as control intervention traditional physical therapy [69,70,71,73,77] and UC [72,73,74,75,76].
According to outcomes measures, data for functional balance assessment were provided by six studies [69,70,71,72,73,74] from the Pediatric Balance Scale (PBS) and of the Bruininks–Oseretsky Test of Motor Proficiency 2’s (BOT-2); dynamic balance was assessed with data from the Timed-Up and Go Test (TUG) [69,74,77]; and static balance was assessed with posturographic parameters [70,75]. Finally, muscular endurance involved studies providing data from the 30 s Chair Stand Test (30-SCST), the Five-times Sit-to-Stand test (5-TSS), and the BOT-2 (strength dimension). All measurements informed about immediate post-intervention.
Finally, none of the included RCTs received external funding to perform the research. Table 2 shows the characteristics of the studies included in the meta-analysis.

3.3. Methodological Quality and Risk of Bias Assessments

The mean methodological quality of the studies included was good, showing a mean score in the PEDro scale of 6.3 ± 1.2 points. Eight studies (89% of all) presented good methodological quality [69,70,72,73,74,75,76,77] and only one moderate [71]. The mean risk of bias in these studies was medium, and selection, performance, and detection were the most reported biases. Selection bias was identified in seven studies (77.7%) due to an inadequate concealed allocation (item 3 not met) [70,71,72,73,74,75,76]; performance bias was present in all studies due to the fact that participants and therapists could not be blinded (items 5 and 6 not met); and finally, detection bias was showed in five studies (55.5%) because evaluators were not blinded (item 7 not met) [69,70,71,72,75]. Table 3 showed in detail the PEDro assessment and bias reported for each study included.

3.4. Meta-Analyses

The studies included in the review provided statistical data to perform four meta-analyses (three for balance variables and another for muscular endurance). The findings of each meta-analysis have been summarized in Table 4.

3.4.1. Functional Balance

The effectiveness of VRBT on functional balance was assessed, including six studies with seven independent comparisons [69,70,71,72,73,74] that provided data from 319 subjects with DS (31.7 per comparison). Our meta-analysis reported low-quality evidence of a large effect (SMD = 1.22; 95% CI 0.64 to 1.81; p < 0.001) favoring VRBT (Figure 2) without heterogeneity (I2 = 0%; Q = 4.2; df = 6; p = 0.38) or risk of publication bias (Egger p = 0.38 in Figure S1). Additionally, our findings showed an increase of 6.4 points (95% CI 1.6 to 11.12; p = 0.009) in the PBS compared to the controls. No variations were found using sensitivity analyses.
In subgroup analyses, on the one hand, meta-regression did not reveal differences between comparison therapies (p = 0.61) (Figure S2) and between children and adolescents (Figure S3).

3.4.2. Dynamic Balance

Three studies with three independent comparisons [69,74,77] provided data from 95 participants with DS (31.7 per study) regarding the effectiveness of VRBT on dynamic balance. Our meta-analysis showed with very low-quality evidence that a large effect (SMD = −2.2; 95% CI −3.1 to −1.25; p < 0.001) favors VRBT (Figure 3) in increasing dynamic balance with moderate heterogeneity (I2 = 27.1%; Q = 2.7; df = 2; p = 0.3) and without risk of publication bias (Egger p = 0.42 in Figure S4). The meta-analysis showed that VRBT is able to reduce by 3.65 s (95% CI −4.81 to −2.48; p < 0.001) the performance of the TUG in comparison to the control intervention. No substantial differences were found after the sensitivity analysis.

3.4.3. Static Balance (Posturographic Postural Control)

The ability to maintain the static balance after VRBT was assessed, including two studies with two independent comparisons [70,75] that provided data from 38 participants (19 per study) per eye condition. Our meta-analysis did not report statistically significant differences between VRBT and the controls in improving static balance in OE (SMD = 0.53; 95% CI −1.1 to 2.2; p = 0.52; I2 = 18.5%; Q = 1.2; df = 1; p = 0.3) and CE (SMD = −0.75; 95% CI −2.37 to 0.87; p = 0.36; I2 = 0%; Q = 0.7; df = 1; p = 0.4) (Figure 4).

3.4.4. Muscular Endurance

The effect of VRBT on muscular endurance was assessed, including four studies with five independent comparisons that provide data from 314 participants (62.8 per study) [69,73,76,77]. The meta-analysis showed low-quality evidence of a large effect (SMD = 1.37; 95% CI 0.58 to 2.2; p < 0.001) favoring VRBT in increasing muscular endurance (Figure 5) without heterogeneity (I2 = 0%; Q = 3.7; df = 4; p = 0.4) or risk of publication bias (Egger p = 0.38 in Figure S5). The sensitivity analysis did not show variation in the pooled effect.
In subgroup analyses, according to specific comparisons, in increasing muscular endurance, VRBT was better than UC (SMD = 1.8; 95% CI 0.41 to 3.1; p < 0.001) but not than CT (SMD = 1.1; 95% CI −0.02 to 2.22; p = 0.053). Additionally, the meta-regression (p = 0.23) did not show differences between children and adolescents (Figure S6).

4. Discussion

Children and adolescents with Down syndrome often exhibit balance and muscle strength deficits [78]. VRBT has shown promise in addressing these impairments [79]. Previous reviews, including those by Lopes et al. (2020), included only two studies [37]; Stander et al. (2021), and Alba-Rueda et al. (2022), who included in their systematic reviews children, adolescents, and adults with DS, suggested that VRBT is a potentially effective therapeutic intervention for this population [38,39]. In addition, the only meta-analysis published to date included studies published up to 2021 [39]. However, recent studies published since 2021 and the need for a more homogeneous intervention group, including only children and adolescents with DS, prompted us to update the literature search and conduct a new meta-analysis. Previous reviews, including those by Lopes et al. (2020), Stander et al. (2021), and Alba-Rueda et al. (2022), have suggested VRBT as a potentially effective therapeutic intervention for this population. However, recent studies published since 2021 and the need for a more homogeneous intervention group prompted us to update the literature search and conduct a new meta-analysis. Therefore, the primary objective of this meta-analysis was to evaluate the efficacy of VRBT in improving balance and muscular endurance in children and adolescents with DS. Secondary objectives included comparing VRBT’s effectiveness to UC or CT and examining potential differences in outcomes between children and adolescents.
Following an updated literature search, we identified three additional studies published in 2023 [77] and 2024 [70,74] that met our inclusion criteria. Finally, our meta-analysis included nine studies providing data from 476 individuals, all children and adolescents with DS. Compared to previous reviews, the quality of evidence and generalizability of our meta-analysis were significantly enhanced due to the increased number of studies and participants. Furthermore, the sample was more homogenous after excluding two studies that included adults with DS [67,68]. Overall, our meta-analysis demonstrated that VRBT is an effective therapy for improving balance and muscular endurance in this population.
The primary outcome evaluated in this meta-analysis was the effectiveness of VRBT in enhancing balance, focusing on three specific dimensions: functional, dynamic, and posturographic static balance. The meta-analyses revealed that VRBT is highly effective in increasing functional and dynamic balance in comparison to CT or UC interventions. An additional analysis confirmed the clinical relevance of these improvements, with VRBT leading to a significant increase of 6.4 points in the PBS [69,70,72,74] and a reduction of 3.65 s in the TUG test [69,74,77]. While the MCID for the PBS and TUG has not been specifically calculated for children with DS, these results exceed the MCID values reported in similar populations for the PBS (5.83 points) and TUG (2.01 s) [80,81]. Both results are in line with the meta-analysis of Alba-Rueda et al. (2022), who showed that VRBT is better than other interventions (CT or UC) in improving functional and dynamic balance in patients of all age groups [39]. However, our meta-analysis differs in including two studies recently published for functional balance [70,74] and another for dynamic balance [77], and it excludes adults with DS and other studies that really did not provide data from functional [75] and dynamic balance assessed with the TUG [72,73,75,76] as they do. Subgroup analyses further confirmed the effectiveness of VRBT over the control or usual care interventions regardless of age (children or adolescents), highlighting its potential for both groups. Regarding static balance, VRBT was not better than others in improving postural control assessed with CoP excursion and Romberg’s test. This result may be attributed to the limited number of studies included in this analysis [70,75]. Further research with additional studies is needed to clarify the effects of VRBT on static balance in this population.
The final meta-analysis of our review demonstrated that VRBT increases muscular endurance in these patients without notable differences between children and adolescents. This suggests that VRBT can be an effective therapy for improving muscular endurance in these age groups. These results align with the meta-analysis by Alba-Rueda et al. (2022), although our meta-analysis included two studies more [69,77], excluding adults with DS [67,68]. A noteworthy finding from our subgroup analysis is that VRBT was superior to UC but not to CT. This implies that in clinical practice, physiotherapists may benefit from combining strength exercises using CT with VRBT to enhance dynamic balance.
The significant improvements observed in balance and muscular endurance can be attributed to several factors. First, all participants involved carried out physical exercises using video games, which have a large ludic component. These video games are named exergames, defined as video games that require body movements to play and function as a form of physical activity [82,83]. The gamification and immersive, ludic, and virtual environments of exergames are key advantages of VRBT, as they increase motivation and adherence to therapy [84]. The continuous challenges offered by these games also enhance curiosity, leading to greater engagement and physical activity, which can improve muscular endurance and balance. While 90% of the VRBT interventions used by the participants were non-immersive, primarily using the Nintendo Wii, these devices are characterized by their ease of use and comprehension, making them suitable for children with specific neurological conditions like DS or cerebral palsy [85,86]. Exergames such as Wii Sports, in which participants play tennis, golf, baseball, sky, soccer, or jumping, require global movements oriented toward functional tasks in the standing position. The repetitive practice of these movements can enhance muscular endurance. Another advantage of a VR device is that it provides somatosensory information (vestibular, auditory, visual, and proprioceptive) essential for maintaining and recovering balance [87]. The low postural control observed in these individuals, often due to hypotonia, muscle weakness and fatigue, and joint laxity, can reduce the gross motor skills and proprioceptive necessary for balance maintenance [74]. VR can address these challenges by inducing neuroplasticity. The multi-sensory inputs received by the brain during VR experiences can lead to neural changes that improve adaptive responses within the central nervous system [88]. Another advantage of VR devices is that they allow for customized therapies focused on patients receiving specific sensory stimuli related to the specific disability to recover from it (global movements, strength, balance, or cognitive tasks) [89]. Finally, the use of non-immersive VR devices, which are typically affordable and easy to use, allows individuals to perform these exercises at home. With proper instruction, parents or caregivers can supervise the activities carried out by children or adolescents [90].
To accurately interpret and generalize our findings, some limitations must be acknowledged. First, the relatively small number of studies included for certain variables and the limited sample sizes of individual studies reduce the quality of evidence, precision, and generalizability of our findings according to GRADE criteria. However, these studies represent the only published research that met our inclusion criteria, demonstrating the effectiveness of our search strategy. Another limitation is the medium risk of bias in some of the studies included, and selection, performance, and detection were the most reported biases that can affect the quality of evidence, accuracy, and generalization of our findings [91,92]. Regarding publication bias, it could not be assessed in meta-analyses with two or fewer studies due to limitations of the statistical software used. It is important to declare the impossibility of assessing if the effectiveness of VRBT will be sustained over time (follow-up). Ninety percent of the studies included used non-immersive VR devices, and these findings can be more supported by the use of non-immersive VR that require a lower level of complexity in its use. Finally, we were unable to assess the quality of evidence regarding the combined effect of CT and VRBT on improving balance in these children. We encourage researchers to perform future studies controlling the possible biases involved with a major sample size and using immersive VR devices and to assess if the effectiveness on balance and muscular endurance is major when CT approaches and VRBT protocols are applied together.

5. Conclusions

This meta-analysis, the first to focus exclusively on children and adolescents with DS, reveals that VRBT is effective in improving balance, particularly functional and dynamic balance, and muscular endurance in this population. While caution is warranted due to the limited number of studies included for certain variables, VRBT emerges as an effective and safe therapeutic option. The engaging and motivating nature of video games used to facilitate physical exercises enhances its appeal. Future research with larger sample sizes and the incorporation of immersive VR devices is necessary to solidify these findings.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/bioengineering11111112/s1, Figure S1: Funnel plot for functional balance (overall); Figure S2: Scatterplot of SMD on therapy comparisons (functional balance); Figure S3: Scatterplot of SMD on age groups (functional balance); Figure S4: Funnel plot for dynamic balance (overall); Figure S5: Funnel plot for functional balance (overall); and Figure S6: Scatterplot of SMD on therapy comparisons (muscular endurance).

Author Contributions

Conceptualization, M.P.-L., I.C.-P., Á.D.-F., M.d.A.M.-I., A.S.-V. and E.O.-G.; methodology, M.P.-L., I.C.-P. and E.O.-G.; software, M.P.-L., I.C.-P. and E.O.-G.; validation, M.P.-L., I.C.-P., Á.D.-F., M.d.A.M.-I., A.S.-V. and E.O.-G.; formal analysis, I.C.-P. and E.O.-G.; investigation, M.P.-L., I.C.-P., Á.D.-F., M.d.A.M.-I., A.S.-V. and E.O.-G.; resources, E.O.-G.; data curation, M.P.-L., I.C.-P., Á.D.-F. and E.O.-G.; writing—original draft preparation, M.P.-L. and I.C.-P.; writing—review and editing, Á.D.-F. and E.O.-G.; visualization, M.P.-L., I.C.-P., Á.D.-F., M.d.A.M.-I., A.S.-V. and E.O.-G.; supervision, I.C.-P. and E.O.-G.; project administration, E.O.-G. All authors have read and agreed to the published version of the manuscript.

Funding

This study received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data will be made available upon reasonable request to the corresponding author.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Bull, M.J. Down Syndrome. N. Engl. J. Med. 2020, 382, 2344–2352. [Google Scholar] [CrossRef] [PubMed]
  2. Baburamani, A.A.; Patkee, P.A.; Arichi, T.; Rutherford, M.A. New approaches to studying early brain development in Down syndrome. Dev. Med. Child Neurol. 2019, 61, 867–879. [Google Scholar] [CrossRef] [PubMed]
  3. Huang, T.; Fakurazi, S.; Cheah, P.-S.; Ling, K.-H. Chromosomal and cellular therapeutic approaches for Down syndrome: A research update. Biochem. Biophys. Res. Commun. 2024, 735, 150664. [Google Scholar] [CrossRef]
  4. Vandoni, M.; Giuriato, M.; Pirazzi, A.; Zanelli, S.; Gaboardi, F.; Carnevale Pellino, V.; Gazzarri, A.A.; Baldassarre, P.; Zuccotti, G.; Calcaterra, V. Motor Skills and Executive Functions in Pediatric Patients with Down Syndrome: A Challenge for Tailoring Physical Activity Interventions. Pediatr. Rep. 2023, 15, 691–706. [Google Scholar] [CrossRef] [PubMed]
  5. Schieve, L.A.; Boulet, S.L.; Boyle, C.; Rasmussen, S.A.; Schendel, D. Health of Children 3 to 17 Years of Age with Down Syndrome in the 1997–2005 National Health Interview Survey. Pediatrics 2009, 123, e253–e260. [Google Scholar] [CrossRef]
  6. Verstegen, R.H.J.; Kusters, M.A.A. Inborn Errors of Adaptive Immunity in Down Syndrome. J. Clin. Immunol. 2020, 40, 791–806. [Google Scholar] [CrossRef]
  7. Mannion, A.; Neil, N.; Fiani, T.; Athamanah, L.; Lyons, J.; McDonagh, K.; Boland, E.; Cooney, R.; Lynch, M.; Youssef, M.; et al. An investigation of sleep problems, gastrointestinal symptoms, comorbid psychopathology and challenging behavior in children and adolescents with Down Syndrome. Res. Dev. Disabil. 2024, 151, 104788. [Google Scholar] [CrossRef]
  8. Cho, Y.; Kwon, Y.; DelRosso, L.; Sobremonte-King, M. Dysphagia severity is associated with worse sleep-disordered breathing in infants with Down syndrome. J. Clin. Sleep Med. 2023, 19, 883–887. [Google Scholar] [CrossRef] [PubMed]
  9. Bala, U.; Leong, M.P.-Y.; Lim, C.L.; Shahar, H.K.; Othman, F.; Lai, M.-I.; Law, Z.-K.; Ramli, K.; Htwe, O.; Ling, K.-H.; et al. Defects in nerve conduction velocity and different muscle fibre-type specificity contribute to muscle weakness in Ts1Cje Down syndrome mouse model. PLoS ONE 2018, 13, e0197711. [Google Scholar] [CrossRef]
  10. Maïano, C.; Hue, O.; Lepage, G.; Morin, A.J.S.; Tracey, D.; Moullec, G. Do Exercise Interventions Improve Balance for Children and Adolescents With Down Syndrome? A Systematic Review. Phys. Ther. 2019, 99, 507–518. [Google Scholar] [CrossRef]
  11. Ghaeeni, S.; Bahari, Z.; Khazaei, A.A. Effect of core stability training on static balance of the children with Down syndrome. Phys. Treat. Phys. Ther. J. 2015, 5, 49–54. [Google Scholar]
  12. Aleksander-Szymanowicz, P.; Filar-Mierzwa, K.; Skiba, A. Effect of dance movement therapy on balance in adults with Down Syndrome. A pilot study. J. Intellect. Disabil. 2023. [Google Scholar] [CrossRef]
  13. Pua, Y.-H.; Ong, P.-H.; Clark, R.A.; Matcher, D.B.; Lim, E.C.-W. Falls efficacy, postural balance, and risk for falls in older adults with falls-related emergency department visits: Prospective cohort study. BMC Geriatr. 2017, 17, 291. [Google Scholar] [CrossRef]
  14. Tsimaras, V.K.; Fotiadou, E.G. Effect of Training on the Muscle Strength and Dynamic Balance Ability of Adults With Down Syndrome. J. Strength Cond. Res. 2004, 18, 343. [Google Scholar] [CrossRef]
  15. de Graaf, G.; Buckley, F.; Skotko, B.G. Estimates of the live births, natural losses, and elective terminations with Down syndrome in the United States. Am. J. Med. Genet. Part A 2015, 167, 756–767. [Google Scholar] [CrossRef] [PubMed]
  16. Bu, Q.; Qiang, R.; Cheng, H.; Wang, A.; Chen, H.; Pan, Z. Analysis of the Global Disease Burden of Down Syndrome Using YLDs, YLLs, and DALYs Based on the Global Burden of Disease 2019 Data. Front. Pediatr. 2022, 10, 882722. [Google Scholar] [CrossRef]
  17. Horak, F.B. Postural orientation and equilibrium: What do we need to know about neural control of balance to prevent falls? Age Ageing 2006, 35 (Suppl. 2), ii7–ii11. [Google Scholar] [CrossRef] [PubMed]
  18. Atalan Efkere, P.; Tarsuslu, T. The effects of Kinesio taping on static and dynamic balance in children with down syndrome: A randomized controlled trial. Somatosens. Mot. Res. 2024, 41, 115–122. [Google Scholar] [CrossRef] [PubMed]
  19. Ruiz-González, L.; Lucena-Antón, D.; Salazar, A.; Martín-Valero, R.; Moral-Munoz, J.A. Physical therapy in Down syndrome: Systematic review and meta-analysis. J. Intellect. Disabil. Res. 2019, 63, 1041–1067. [Google Scholar] [CrossRef]
  20. Büyükçelik, N.M.; Yiğit, S.; Turhan, B. An investigation of the effects of dual-task balance exercises on balance, functional status and dual-task performance in children with Down syndrome. Dev. Neurorehabil. 2023, 26, 320–327. [Google Scholar] [CrossRef]
  21. Takahashi, H.; An, M.; Sasai, T.; Seki, M.; Matsumura, T.; Ogawa, Y.; Matsushima, K.; Tabata, A.; Kato, T. The effectiveness of dance movement therapy for individuals with Down syndrome: A pilot randomised controlled trial. J. Intellect. Disabil. Res. 2023, 67, 640–654. [Google Scholar] [CrossRef] [PubMed]
  22. Purpura, G.; Di Giusto, V.; Zorzi, C.F.; Figliano, G.; Randazzo, M.; Volpicelli, V.; Blonda, R.; Brazzoli, E.; Reina, T.; Rezzonico, S.; et al. Use of Virtual Reality in School-Aged Children with Developmental Coordination Disorder: A Novel Approach. Sensors 2024, 24, 5578. [Google Scholar] [CrossRef] [PubMed]
  23. Arman, N.; Tarakci, E.; Tarakci, D.; Kasapcopur, O. Effects of Video Games–Based Task-Oriented Activity Training (Xbox 360 Kinect) on Activity Performance and Participation in Patients With Juvenile Idiopathic Arthritis. Am. J. Phys. Med. Rehabil. 2019, 98, 174–181. [Google Scholar] [CrossRef] [PubMed]
  24. Tobaiqi, M.A.; Albadawi, E.A.; Fadlalmola, H.A.; Albadrani, M.S. Application of Virtual Reality-Assisted Exergaming on the Rehabilitation of Children with Cerebral Palsy: A Systematic Review and Meta-Analysis. J. Clin. Med. 2023, 12, 7091. [Google Scholar] [CrossRef] [PubMed]
  25. Sánchez-Caballero, E.; Ortega-Donaire, L.; Sanz-Martos, S. Immersive Virtual Reality for Pain and Anxiety Management Associated with Medical Procedures in Children and Adolescents: A Systematic Review. Children 2024, 11, 975. [Google Scholar] [CrossRef]
  26. Bateni, H.; Carruthers, J.; Mohan, R.; Pishva, S. Use of Virtual Reality in Physical Therapy as an Intervention and Diagnostic Tool. Rehabil. Res. Pract. 2024, 2024, 1122286. [Google Scholar] [CrossRef]
  27. Lee, H.-S.; Lim, J.-H.; Jeon, B.-H.; Song, C.-S. Non-immersive Virtual Reality Rehabilitation Applied to a Task-oriented Approach for Stroke Patients: A Randomized Controlled Trial. Restor. Neurol. Neurosci. 2020, 38, 165–172. [Google Scholar] [CrossRef]
  28. Palacios-Navarro, G.; Hogan, N. Head-Mounted Display-Based Therapies for Adults Post-Stroke: A Systematic Review and Meta-Analysis. Sensors 2021, 21, 1111. [Google Scholar] [CrossRef]
  29. Matallaoui, A.; Koivisto, J.; Hamari, J.; Zarnekow, R. How effective is “exergamification”? A systematic review on the effectiveness of gamification features in exergames. In Proceedings of the 50th Hawaii International Conference on System Sciences, Hilton Waikoloa Village, HI, USA, 4–7 January 2017. [Google Scholar]
  30. Holden, M.K. Virtual environments for motor rehabilitation. Cyberpsychol. Behav. 2005, 8, 187–211. [Google Scholar] [CrossRef]
  31. Merians, A.S.; Tunik, E.; Adamovich, S.V. Virtual reality to maximize function for hand and arm rehabilitation: Exploration of neural mechanisms. Stud. Health Technol. Inform. 2009, 145, 109–125. [Google Scholar] [CrossRef]
  32. Maggio, M.G.; Valeri, M.C.; De Luca, R.; Di Iulio, F.; Ciancarelli, I.; De Francesco, M.; Calabrò, R.S.; Morone, G. The Role of Immersive Virtual Reality Interventions in Pediatric Cerebral Palsy: A Systematic Review across Motor and Cognitive Domains. Brain Sci. 2024, 14, 490. [Google Scholar] [CrossRef] [PubMed]
  33. Berg, P.; Becker, T.; Martian, A.; Danielle, P.K.; Wingen, J. Motor Control Outcomes Following Nintendo Wii Use by a Child With Down Syndrome. Pediatr. Phys. Ther. 2012, 24, 78–84. [Google Scholar] [CrossRef] [PubMed]
  34. Corey, J.; Tsai, J.M.; Mhadeshwar, A.; Srinivasan, S.; Bhat, A. Digital motor intervention effects on physical activity performance of individuals with developmental disabilities: A systematic review. Disabil. Rehabil. 2024, 1–16. [Google Scholar] [CrossRef] [PubMed]
  35. de Menezes, L.D.C.; Massetti, T.; Oliveira, F.R.; de Abreu, L.C.; Malheiros, S.R.P.; Trevizan, I.L.; Moriyama, C.H.; de Mello Monteiro, C.B. Motor learning and virtual reality in Down syndrome; a literature review. Int. Arch. Med. 2015, 8. [Google Scholar] [CrossRef]
  36. Mohamed, R.A.; Abdel-Rahman, S.; Aly, M.G. Virtual reality for motor rehabilitation of children with Down syndrome: Systematic review. Med. J. Cairo Univ. 2019, 87, 1117–1123. [Google Scholar]
  37. Lopes, J.B.P.; de Almeida Carvalho Duarte, N.; Lazzari, R.D.; Oliveira, C.S. Virtual reality in the rehabilitation process for individuals with cerebral palsy and Down syndrome: A systematic review. J. Bodyw. Mov. Ther. 2020, 24, 479–483. [Google Scholar] [CrossRef]
  38. Stander, J.; du Preez, J.C.; Kritzinger, C.; Obermeyer, N.M.; Struwig, S.; van Wyk, N.; Zaayman, J.; Burger, M. Effect of virtual reality therapy, combined with physiotherapy for improving motor proficiency in individuals with Down syndrome: A systematic review. S. Afr. J. Physiother. 2021, 77, 1516. [Google Scholar] [CrossRef]
  39. Alba-Rueda, A.; Moral-Munoz, J.A.; De Miguel-Rubio, A.; Lucena-Anton, D. Exergaming for Physical Therapy in Patients with Down Syndrome: A Systematic Review and Meta-Analysis of Randomized-Controlled Trials. Games Health J. 2022, 11, 67–78. [Google Scholar] [CrossRef]
  40. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
  41. Higgins, J.; Green, S. Cochrane Handbook for Systematic Reviews of Interventions; John Wiley & Sons: London, UK, 2011. [Google Scholar]
  42. Cooper, H.; Hedges, L.; Valentine, J.C. The Handbook of Research Synthesis and Meta-Analysis; Russell Sage Foundation: New York, NY, USA, 2009. [Google Scholar]
  43. Shea, B.J.; Reeves, B.C.; Wells, G.; Thuku, M.; Hamel, C.; Moran, J.; Moher, D.; Tugwell, P.; Welch, V.; Kristjansson, E.; et al. AMSTAR 2: A critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 2017, 358, j4008. [Google Scholar] [CrossRef]
  44. Amir-Behghadami, M.; Janati, A. Population, Intervention, Comparison, Outcomes and Study (PICOS) design as a framework to formulate eligibility criteria in systematic reviews. Emerg. Med. J. 2020, 37, 387. [Google Scholar] [CrossRef] [PubMed]
  45. Cohen, J. A Coefficient of Agreement for Nominal Scales. Educ. Psychol. Meas. 1960, 20, 37–46. [Google Scholar] [CrossRef]
  46. Landis, J.R.; Koch, G.G. The Measurement of Observer Agreement for Categorical Data. Biometrics 1977, 33, 159. [Google Scholar] [CrossRef]
  47. Hozo, S.P.; Djulbegovic, B.; Hozo, I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med. Res. Methodol. 2005, 5, 13. [Google Scholar] [CrossRef] [PubMed]
  48. Berg, K.O.; Maki, B.E.; Williams, J.I.; Holliday, P.J.; Wood-Dauphinee, S.L. Clinical and laboratory measures of postural balance in an elderly population. Arch. Phys. Med. Rehabil. 1992, 73, 1073–1080. [Google Scholar]
  49. Podsiadlo, D.; Richardson, S. The timed “Up & Go”: A test of basic functional mobility for frail elderly persons. J. Am. Geriatr. Soc. 1991, 39, 142–148. [Google Scholar] [CrossRef]
  50. Noamani, A.; Riahi, N.; Vette, A.H.; Rouhani, H. Clinical Static Balance Assessment: A Narrative Review of Traditional and IMU-Based Posturography in Older Adults and Individuals with Incomplete Spinal Cord Injury. Sensors 2023, 23, 8881. [Google Scholar] [CrossRef]
  51. Booth, F.W.; Ruegsegger, G.N.; Toedebusch, R.G.; Yan, Z. Endurance Exercise and the Regulation of Skeletal Muscle Metabolism. Prog. Mol. Biol. Transl. Sci. 2015, 135, 129–151. [Google Scholar]
  52. Maher, C.G.; Sherrington, C.; Herbert, R.D.; Moseley, A.M.; Elkins, M. Reliability of the PEDro scale for rating quality of randomized controlled trials. Phys. Ther. 2003, 83, 713–721. [Google Scholar] [CrossRef]
  53. Verhagen, A.P.; de Vet, H.C.; de Bie, R.A.; Kessels, A.G.; Boers, M.; Bouter, L.M.; Knipschild, P.G. The Delphi list: A criteria list for quality assessment of randomized clinical trials for conducting systematic reviews developed by Delphi consensus. J. Clin. Epidemiol. 1998, 51, 1235–1241. [Google Scholar] [CrossRef]
  54. Gonzalez, G.Z.; Moseley, A.M.; Maher, C.G.; Nascimento, D.P.; da Cunha Menezes Costa, L.; Costa, L.O. Methodologic Quality and Statistical Reporting of Physical Therapy Randomized Controlled Trials Relevant to Musculoskeletal Conditions. Arch. Phys. Med. Rehabil. 2018, 99, 129–136. [Google Scholar] [CrossRef] [PubMed]
  55. Atkins, D.; Best, D.; Briss, P.A.; Eccles, M.; Falck-Ytter, Y.; Flottorp, S.; Guyatt, G.H.; Harbour, R.T. Grading quality of evidence and strength of recommendations. BMJ 2004, 328, 1490. [Google Scholar] [CrossRef] [PubMed]
  56. Schuünemann, H.; Brozżek, J.; Guyatt, G.; Oxman, A. Manual GRADE (Grading of Recommendations, Assessment, Development and Evaluation); Javierana GRADE Center: Bogotá, Colombia, 2017. [Google Scholar]
  57. Meader, N.; King, K.; Llewellyn, A.; Norman, G.; Brown, J.; Rodgers, M.; Moe-Byrne, T.; Higgins, J.P.; Sowden, A.; Stewart, G. A checklist designed to aid consistency and reproducibility of GRADE assessments: Development and pilot validation. Syst. Rev. 2014, 3, 82. [Google Scholar] [CrossRef]
  58. Borenstein, M.; Hedges, L.; Higgins, J.; Rothstein, H. Comprehensive Meta-Analysis Software. version 4; Biostat: Englewood, NY, USA, 2023. [Google Scholar]
  59. Cohen, J. Statistical Power Analysis for the Behavioral Sciences; Academic Press: New York, NY, USA, 1977. [Google Scholar]
  60. DerSimonian, R.; Laird, N. Meta-analysis in clinical trials. Control. Clin. Trials 1986, 7, 177–188. [Google Scholar] [CrossRef]
  61. Rücker, G.; Schwarzer, G. Beyond the forest plot: The drapery plot. Res. Synth. Methods 2021, 12, 13–19. [Google Scholar] [CrossRef]
  62. Kinney, A.R.; Eakman, A.M.; Graham, J.E. Novel Effect Size Interpretation Guidelines and an Evaluation of Statistical Power in Rehabilitation Research. Arch. Phys. Med. Rehabil. 2020, 101, 2219–2226. [Google Scholar] [CrossRef]
  63. Copay, A.G.; Subach, B.R.; Glassman, S.D.; Polly, D.W.; Schuler, T.C. Understanding the minimum clinically important difference: A review of concepts and methods. Spine J. 2007, 7, 541–546. [Google Scholar] [CrossRef]
  64. Man-Son-Hing, M.; Laupacis, A.; O’Rourke, K.; Molnar, F.J.; Mahon, J.; Chan, K.B.Y.; Wells, G. Determination of the clinical importance of study results. J. Gen. Intern. Med. 2002, 17, 469–476. [Google Scholar] [CrossRef] [PubMed]
  65. Higgins, J.; Thompson, S.; Altman, D. Statistical heterogeneity in systematic reviews of clinical trials: A critical appraisal of guidelines and practice. J. Health Serv. Res. Policy 2002, 7, 51–61. [Google Scholar] [CrossRef]
  66. Higgins, J.P.T.; Thompson, S.G.; Deeks, J.J.; Altman, D.G. Measuring inconsistency in meta-analyses. BMJ 2003, 327, 557–560. [Google Scholar] [CrossRef]
  67. Perrot, A.; Maillot, P.; Le Foulon, A.; Rebillat, A.-S. Effect of Exergaming on Physical Fitness, Functional Mobility, and Cognitive Functioning in Adults With Down Syndrome. Am. J. Intellect. Dev. Disabil. 2021, 126, 34–44. [Google Scholar] [CrossRef] [PubMed]
  68. Silva, V.; Campos, C.; Sá, A.; Cavadas, M.; Pinto, J.; Simões, P.; Machado, S.; Murillo-Rodríguez, E.; Barbosa-Rocha, N. Wii-based exercise program to improve physical fitness, motor proficiency and functional mobility in adults with Down syndrome. J. Intellect. Disabil. Res. 2017, 61, 755–765. [Google Scholar] [CrossRef]
  69. Abdel Ghafar, M.A.; Abdelraouf, O.R. Effect of virtual reality versus traditional physical therapy on functional balance in children with Down Syndrome: A randomized comparative study. Int. J. Physiother. Res. 2017, 5, 2088–2094. [Google Scholar] [CrossRef]
  70. Memon, A.G.; Ali, S.; Adnan, Q.; Tahir, S. Effects of Virtual Reality on Static and Dynamic Balance among Individuals with Down Syndrome. J. Liaquat Univ. Med. Health Sci. 2024, 23, 116–120. [Google Scholar]
  71. Rahman, S.A.; Rahman, A. Efficacy of virtual reality-based therapy on balance in children with Down syndrome. World Appl. Sci. J. 2010, 10, 254–261. [Google Scholar]
  72. Reis, J.R.G.; Neiva, C.M.; Pessoa Filho, D.M.; Ciolac, E.G.; Verardi, C.E.L.; da Cruz Siqueira, L.O.; de Freitas Gonçalves, D.; da Silva, G.R.; Hiraga, C.Y.; Tonello, M.G.M. Virtual reality therapy: Motor coordination and balance analysis in children and teenagers with Down syndrome. Eur. J. Hum. Mov. 2017, 38, 53–67. [Google Scholar]
  73. Wuang, Y.P.; Chiang, C.S.; Su, C.Y.; Wang, C.C. Effectiveness of virtual reality using Wii gaming technology in children with Down syndrome. Res. Dev. Disabil. 2011, 32, 312–321. [Google Scholar] [CrossRef]
  74. Yunus, F.T.; Widagda, I.M.; Isma, R. The Effect Of Sensory-Motor Virtual Reality on Balance in Children with Clinical Down Syndrome. J. Kedokt. Diponegoro (Diponegoro Med. J.) 2024, 13, 66–71. [Google Scholar] [CrossRef]
  75. Gómez Álvarez, N.; Venegas Mortecinos, A.; Zapata Rodríguez, V.; López Fontanilla, M.; Maudier Vásquez, M.; Pavez-Adasme, G.; Hemández-Mosqueira, C. Efecto de una intervención basada en realidad virtual sobre las habi lidades motrices básicas y control postural de niños con Síndrome de Down. Rev. Chil. Pediatría 2018, 89, 747–752. [Google Scholar] [CrossRef]
  76. Lin, H.-C.; Wuang, Y.-P. Strength and agility training in adolescents with Down syndrome: A randomized controlled trial. Res. Dev. Disabil. 2012, 33, 2236–2244. [Google Scholar] [CrossRef]
  77. Suarez-Villadat, B.; Sadarangani, K.P.; Villagra, A. Effectiveness of exergames programme to modify body composition and health-related physical fitness in adolescents with down syndrome after COVID-19 quarantine. Eur. J. Sport Sci. 2023, 23, 2210–2220. [Google Scholar] [CrossRef] [PubMed]
  78. AL-Nemr, A.; Reffat, S. Effect of Pilates exercises on balance and gross motor coordination in children with Down syndrome. Acta Neurol. Belg. 2024. [Google Scholar] [CrossRef] [PubMed]
  79. Boato, E.; Melo, G.; Filho, M.; Moresi, E.; Lourenço, C.; Tristão, R. The Use of Virtual and Computational Technologies in the Psychomotor and Cognitive Development of Children with Down Syndrome: A Systematic Literature Review. Int. J. Environ. Res. Public Health 2022, 19, 2955. [Google Scholar] [CrossRef]
  80. Chen, C.; Shen, I.; Chen, C.; Wu, C.; Liu, W.-Y.; Chung, C. Validity, responsiveness, minimal detectable change, and minimal clinically important change of Pediatric Balance Scale in children with cerebral palsy. Res. Dev. Disabil. 2013, 34, 916–922. [Google Scholar] [CrossRef] [PubMed]
  81. Nicolini-Panisson, R.D.; Donadio, M.V.F. Normative values for the Timed “Up and Go” test in children and adolescents and validation for individuals with Down syndrome. Dev. Med. Child Neurol. 2014, 56, 490–497. [Google Scholar] [CrossRef]
  82. Gao, Z.; Lee, J.E.; Pope, Z.; Zhang, D. Effect of Active Videogames on Underserved Children’s Classroom Behaviors, Effort, and Fitness. Games Health J. 2016, 5, 318–324. [Google Scholar] [CrossRef]
  83. Benzing, V.; Schmidt, M. Exergaming for Children and Adolescents: Strengths, Weaknesses, Opportunities and Threats. J. Clin. Med. 2018, 7, 422. [Google Scholar] [CrossRef]
  84. Ju, Y.-J.; Du, Y.-C.; Huang, H.-C.; Hu Kao, P.-S.; Cherng, R.-J. Development and feasibility of a virtual reality-based exergaming program to enhance cardiopulmonary fitness in children with developmental coordination disorder. Front. Pediatr. 2023, 11, 1238471. [Google Scholar] [CrossRef]
  85. Montoro-Cárdenas, D.; Cortés-Pérez, I.; del Rocío Ibancos-Losada, M.; Zagalaz-Anula, N.; Obrero-Gaitán, E.; Osuna-Pérez, M.C. Nintendo® Wii Therapy Improves Upper Extremity Motor Function in Children with Cerebral Palsy: A Systematic Review with Meta-Analysis. Int. J. Environ. Res. Public Health 2022, 19, 12343. [Google Scholar] [CrossRef]
  86. Meriggi, P.; Mandalà, M.; Randazzo, M.; Brazzoli, E.; Castagna, A.; Di Giusto, V.; Cavallini, A.; Marzegan, A.; Lencioni, T.; Olivieri, I. Non-immersive virtual reality based treatment for children with unilateral cerebral palsy: Preliminary results. J. Pediatr. Rehabil. Med. 2024, 17, 107–123. [Google Scholar] [CrossRef]
  87. Huang, D.; Mao, Y.; Chen, P.; Li, L. Virtual reality training improves balance function. Neural Regen. Res. 2014, 9, 1628. [Google Scholar] [CrossRef] [PubMed]
  88. Drigas, A.; Sideraki, A. Brain Neuroplasticity Leveraging Virtual Reality and Brain–Computer Interface Technologies. Sensors 2024, 24, 5725. [Google Scholar] [CrossRef] [PubMed]
  89. Sideraki, A.; Drigas, A. Development of social skills for people with ASD through intervention with digital technologies and virtual reality (VR) tools. Res. Soc. Dev. 2023, 12, e11512541407. [Google Scholar] [CrossRef]
  90. Phelan, I.; Carrion-Plaza, A.; Furness, P.J.; Dimitri, P. Home-based immersive virtual reality physical rehabilitation in paediatric patients for upper limb motor impairment: A feasibility study. Virtual Real. 2023, 27, 3505–3520. [Google Scholar] [CrossRef]
  91. Armijo-Olivo, S.; Saltaji, H.; da Costa, B.R.; Fuentes, J.; Ha, C.; Cummings, G.G. What is the influence of randomisation sequence generation and allocation concealment on treatment effects of physical therapy trials? A meta-epidemiological study. BMJ Open 2015, 5, e008562. [Google Scholar] [CrossRef]
  92. Armijo-Olivo, S.; Fuentes, J.; da Costa, B.R.; Saltaji, H.; Ha, C.; Cummings, G.G. Blinding in Physical Therapy Trials and Its Association with Treatment Effects. Am. J. Phys. Med. Rehabil. 2017, 96, 34–44. [Google Scholar] [CrossRef]
Bioengineering 11 01112 g001
Figure 1. The PRISMA flow diagram for the study selection process.
Figure 1. The PRISMA flow diagram for the study selection process.
Bioengineering 11 01112 g001
Bioengineering 11 01112 g002
Figure 2. The forest plot of the effectiveness of VRBT in increasing functional balance [69,70,71,72,73,74].
Figure 2. The forest plot of the effectiveness of VRBT in increasing functional balance [69,70,71,72,73,74].
Bioengineering 11 01112 g002
Bioengineering 11 01112 g003
Figure 3. The forest plot of the effectiveness of VRBT in increasing dynamic balance [69,74,77].
Figure 3. The forest plot of the effectiveness of VRBT in increasing dynamic balance [69,74,77].
Bioengineering 11 01112 g003
Bioengineering 11 01112 g004
Figure 4. The forest plot of the effectiveness of VRBT in increasing static balance with open and closed eyes [70,75].
Figure 4. The forest plot of the effectiveness of VRBT in increasing static balance with open and closed eyes [70,75].
Bioengineering 11 01112 g004
Bioengineering 11 01112 g005
Figure 5. The forest plot of the effectiveness of VRBT in increasing muscular endurance [69,73,76,77].
Figure 5. The forest plot of the effectiveness of VRBT in increasing muscular endurance [69,73,76,77].
Bioengineering 11 01112 g005
Table 1. Search strategy applied for each database.
Table 1. Search strategy applied for each database.
DatabasesSearch Strategy
PubMed Medline(down syndrome[mh] or down* syndrome[tiab] or syndrome, down [tiab] or trisomy-21[tiab]) AND (virtual reality[mh] or virtual reality[tiab] or reality, virtual[tiab] or virtual reality exposure therapy[mh] or virtual reality exposure therap*[tiab] or virtual reality immersion therap* [tiab] or reality therapy, virtual [tiab] or exergaming[mh] or exergam*[tiab] or virtual reality exercise[tiab] or active-video gam*[tiab])
SCOPUSTITLE-ABS-KEY(“down syndrome” or “syndrome, down” or “trisomy-21”) AND TITLE-ABS-KEY(“virtual reality” or “reality, virtual” or “virtual reality exposure therapy” or “virtual reality immersion therapy” or “reality therapy, virtual” or “exergaming” or “exergame” or “exergames” or “virtual reality exercise” or “active-video game”)
Web of ScienceTOPIC (*down syndrome* or *syndrome, down* or *trisomy-21*) AND TOPIC (*virtual reality* or *reality, virtual* or *virtual reality exposure therapy* or *virtual reality immersion therapy* or *reality therapy, virtual* or *exergaming* or *exergame* or *exergames* or *virtual reality exercise* or *active-video game*)
CINAHL CompleteAB (down syndrome or down, syndrome or trisomia 21) AND AB (virtual reality or reality, virtual or virtual reality exposure therapy or virtual reality immersion therapy or reality therapy, virtual or exergaming or exergame or exergames or virtual reality exercise or active-video game)
PEDroDown syndrome and virtual reality
Table 2. Characteristics of the studies included in the meta-analysis.
Table 2. Characteristics of the studies included in the meta-analysis.
StudyVRBT GroupControl GroupVariable (Test)Qualitative Findings in Individual Studies
Sample CharacteristicsVRBT Intervention CharacteristicsSample CharacteristicsControl Intervention CharacteristicsIntra-Group DifferencesInter-Group Differences
VR SystemDuration of VRBT
Abdel Ghafar, MA et al., 2017 [69] (Saudi Arabia)
Non-single blinded RCT
Setting: Special Education School
Funding: NR		13 children; 7.2 ± 1.9 years; Sex per group ND
ID severity: IQ mild (SBIS)		NIVR device: Nintendo Wii Fit using sports video games.24 sessions, during 8 weeks, 3 per week and 30 min per session13 children; 7.4 ± 1.3 years; Sex per group NDTraditional physical therapy, including balance exercises in standing and sitting positionFunctional balance (PBS)NRStatistically significant differences favors VRBT group (p = 0.046)
Dynamic balance (TUG)NRStatistically significant differences favors VRBT group (p = 0.043)
Muscular endurance
(5-TSS)		NRStatistically significant differences favors VRBT group (p = 0.027)
Gómez-Alvárez, N et al., 2018 [75] (Chile) Non-blinded RCT
Setting: Special Education School
Funding: No		9 children; 8.3 ± 2.1 years; Sex per group ND
ID severity: IQ NR		NIVR device: Nintendo Wii Fit Balance Board using sports video games.10 sessions, during 5 weeks, twice per week, and 20 min per session7 children; 8.4 ± 1.6 years; Sex per group NDUsual care daily routineStatic balance (posturograpy)Statistically significant intragroup differences in VRBT for closed eyes assessment (p = 0.039)Not statistically significant differences between groups in any open and closed eyes condition (p > 0.05)
Lin, HC and Wang, YP 2012 [76] (Taiwan) Single-blind RCTSetting: University
Funding: NR		46 adolescents, 15.6 ± 3.6 years;
21B:25G
ID severity: IQ 52.5 ± 11.7 (WISC-III)		NIVR device: Nintendo Wii sports video games.18 sessions during 6 weeks, 3 sessions per week, and 20 min per session46 adolescents; 14.9 ± 3.9 years; 22B:24GUsual care daily routineMuscular endurance (BOT-2)NRStatistically significant differences favors VRBT group (p = 0.02)
Memon, AG et al., 2024 [70] (Pakistan) Non-blinded RCT
Setting: Rehabilitation Center
Funding: No		12 children; 8.1 ± 0.8 years; Sex ND
ID severity: IQ 62.5 ± 3.5 (SBIS)		NIVR device: Nintendo Wii Fit using video games.24 sessions during 8 weeks, 3 sessions per week, and 30 min per session12 children; 7.6 ± 0.9 years; Sex NDTraditional physical therapy, including balance exercises in standing and sitting positionFunctional balance (PBS)Statistically significant intragroup differences in VRBT (p = 0.005) and control (p < 0.01) groupsNot statistically significant differences between groups (p = 0.38)
Static balance (posturograpy)Statistically significant intragroup differences in VRBT (p < 0.05) and control (p < 0.05) groupsNot statistically significant differences between groups (p > 0.05)
Rahman, SA et al., 2010 [71] (Egypt)
Non-blinded RCT
Setting: Community association
Funding: NR		15 children; 10.9 ± 1.2 years;
6B:9G
ID severity: IQ 36–67 (SBIS)		NIVR device: Nintendo Wii Fit Balance Board using three sports video games. Additionally, individuals were performing conventional physical therapy exercises.36 sessions during 6 weeks, 6 sessions per week, and 60 min per session15 children; 11.6 ± 0.4 years;
7B:8G		Traditional physical therapy program comprising strengthening, walking, and climbing stairs exercisesFunctional balance
(BOT-2)		Statistically significant intragroup differences in VRBT (p < 0.001) and control (p = 0.017) groupsStatistically significant differences favors VRBT group (p < 0.001)
Reis, JRG et al., 2017 [72] (Brazil)
Non-blinded RCT
Setting: Community association
Funding: NR		7 children;
9 ± 2.5 years;
Sex ND
ID severity: IQ NR		NIVR device: Xbox 360 plus Kinect sensor using two video games (River Rush and Hall of ricochets)16 sessions during 4 weeks, 4 sessions per week, and maximal 20 min per session5 children; 8 ± 2.5 years;
Sex ND		Usual care daily routineFunctional balance (PBS)NRStatistically significant differences favors VRBT group (p = 0.01)
Suarez-Villadat, B et al., 2023 [77] (Spain)
Single-blind RCT
Setting: Special Education School
Funding: NR		24 adolescents;
14.1 ± 1.2 years; 14B:10G
ID severity: mild–moderate		NIVR device: Nintendo Wii Fit using sports video games.60 sessions during 20 weeks, 3 sessions per week, and 60 min per session25 adolescents; 14.3 ± 1 years; 16B:9GTraditional physical therapy program comprising motor and coordination exercises related motor skillsDynamic balance (TUG)Statistically significant intragroup differences in VRBT (p = 0.002)Statistically significant differences favors VRBT group (p = 0.038)
Muscular endurance
(30-SCST)		Statistically significant intragroup differences in VRBT (p = 0.008)Statistically significant differences favors VRBT group (p = 0.027)
Wuang, YP et al., 2011 [73] (Taiwan) Single-blind RCT
Setting: University
Funding: NR		52 children; 7–12 years old (range)
Sex ND
ID severity: IQ NR		NIVR device: Nintendo Wii Fit using sports video games. 48 sessions during 24 weeks, twice per week, and 60 min per session53 children; 7–12 years old (range); Sex NDTraditional physical therapy, including balance exercisesFunctional balance
(BOT-2)		NRNot statistically significant differences between groups (p > 0.05)
50 children; 7–12 years old (range); Sex NDUsual care daily routineMuscular endurance (BOT-2)NRNot statistically significant differences between groups (p > 0.05)
Yunus, FT et al., 2024 [74] (Indonesia)
Single-blind RCT
Setting: University
Funding: No		10 adolescents; 12.9 ± 3.2 years; Sex per group ND
ID severity: IQ score 55–69		IVR device: Head mounted displays SenMor’s VR.8 sessions, during 4 weeks, twice per week, and 20 min per session10 adolescents; 12.9 ± 3.2 years; Sex per group NDUsual care daily routineFunctional balance (PBS)Statistically significant intragroup differences in VRBT (p < 0.001)Statistically significant differences favors VRBT group (p < 0.001)
Dynamic balance (TUG)Statistically significant intragroup differences in VRBT (p < 0.001)Statistically significant differences favors VRBT group (p < 0.001)
Abbreviations: VRBT, virtual reality-based therapy; VR, virtual reality; WISC-III, Wechsler Intelligence Scale for Children—Third Edition; IQ, intelligent quotient; SBIS, Stanford Binet intelligence scale; ND, non-defined; NR, non-reported; NIVR, non-immersive virtual reality; IVR, immersive virtual reality; RCT, randomized controlled trial; B, boys; G, girls; PBS, Pediatric Balance Scale; BOT-2, Bruininks–Oseretsky Test of Motor Proficiency 2; TUG, Timed-Up and Go Test, 30-SCST, 30-s Chair Stand Test; 5-TSS, Five-times Sit-to-Stand test.
Table 3. The PEDro assessment and biases reported in the studies included.
Table 3. The PEDro assessment and biases reported in the studies included.
StudyItemsTotalQualityBiases
1234567891011
Abdel Ghafar, MA et al., 2017 [69]YesYesYesYesNoNoNoYesYesYesYes7/10GoodPerformance and detection
Gómez-Alvárez, N et al., 2018 [75]YesYesNoYesNoNoNoYesYesYesYes6/10GoodSelection, performance, and detection
Lin, HC and Wuang, YP 2012 [76]YesYesNoYesNoNoYesYesYesYesYes7/10GoodSelection and performance
Memon, AG et al., 2024 [70]YesYesNoYesNoNoNoYesYesYesYes6/10GoodSelection, performance, and detection
Rahman, SA et al., 2010 * [71]YesYesNoYesNoNoNoNoNoYesYes4/10ModerateSelection, performance, and detection
Reis, JRG et al., 2017 [72]YesYesNoYesNoNoNoYesYesYesYes6/10GoodSelection, performance, and detection
Suarez-Villadat, B et al., 2023 [77]YesYesYesYesNoNoYesYesYesYesYes8/10GoodPerformance
Wuang, YP et al., 2011 * [73]YesYesNoYesNoNoYesYesNoYesYes6/10GoodSelection and performance
Yunus, FT et al., 2024 [74]YesYesNoYesNoNoYesYesYesYesYes7/10GoodSelection and performance
Abbreviations: 1: Eligibility criteria; 2: random allocation; 3: concealed allocation; 4: baseline comparability; 5: blind subjects; 6: blind therapists; 7: blind assessors: 8: measures of at least one key outcome were obtained from more than 85% of the subjects initially allocated to groups; 9: intention-to-treat analysis; 10: between-group comparisons; 11: point estimates and variability. Note: The eligibility criteria item does not contribute to the total score. Note: The score of the studies marked with * was confirmed in the PEDro database: https://pedro.org.au/spanish/ (accessed on 3–10 September 2024).
Table 4. Main findings in meta-analyses.
Table 4. Main findings in meta-analyses.
Effect SizeHeterogeneityPUBLICATION BIASQuality of Evidence (GRADE)
VariablesKNNsSMD95% CIpQ (df)I2 (p)Funnel Plot (Egger p)Trim and FillRisk of BiasInconsIndirectImprecPub
Bias		Quality
Adj SMD% var
Functional balance731945.61.220.64 to 1.81<0.0014.2 (6)0% (0.65)Sym (0.38)1.220%MediumNoNoYesNoLow
Dynamic balance39531.7−2.2−3.1 to −1.25<0.0012.7 (2)27.1% (0.3)Sym (0.42)−2.150%MediumProb.NoYesNoVery low
Static balance OE238190.53−1.1 to 2.20.521.2 (1)18.5% (0.3)NPNPNPMediumProb.NoYesProb.Very low
Static balance CE23819−0.75−2.37 to 0.870.360.7 (1)0% (0.4)NPNPNPMediumNoNoYesProb.Very low
Muscular endurance531462.81.370.58 to 2.2<0.0013.7 (4)0% (0.4)Sym (0.24)1.370%MediumNoNoYesNoLow
Abbreviations: K, number of comparisons; N, total sample size; Ns, participants per study; SMD, standardized mean difference; 95% CI. 95% confidence interval; p, p-value; Q, Q-test; df, degree of freedom; I2, degree of inconsistency; Adj, adjusted; % var, percentage of variation; RAGT, robotic-assisted gait training; TT, treadmill training; CT, conventional therapy; Funct. Indep, functional independence; NP, not possible to calculate.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Piñar-Lara, M.; Cortés-Pérez, I.; Díaz-Fernández, Á.; Montilla-Ibáñez, M.d.A.; Sedeño-Vidal, A.; Obrero-Gaitán, E. Virtual Reality-Based Therapy Can Enhance Balance and Muscular Endurance in Children and Adolescents with Down Syndrome: A Systematic Review with a Meta-Analysis. Bioengineering 2024, 11, 1112. https://doi.org/10.3390/bioengineering11111112

AMA Style

Piñar-Lara M, Cortés-Pérez I, Díaz-Fernández Á, Montilla-Ibáñez MdA, Sedeño-Vidal A, Obrero-Gaitán E. Virtual Reality-Based Therapy Can Enhance Balance and Muscular Endurance in Children and Adolescents with Down Syndrome: A Systematic Review with a Meta-Analysis. Bioengineering. 2024; 11(11):1112. https://doi.org/10.3390/bioengineering11111112

Chicago/Turabian Style

Piñar-Lara, Marina, Irene Cortés-Pérez, Ángeles Díaz-Fernández, María de Alharilla Montilla-Ibáñez, Ana Sedeño-Vidal, and Esteban Obrero-Gaitán. 2024. "Virtual Reality-Based Therapy Can Enhance Balance and Muscular Endurance in Children and Adolescents with Down Syndrome: A Systematic Review with a Meta-Analysis" Bioengineering 11, no. 11: 1112. https://doi.org/10.3390/bioengineering11111112

APA Style

Piñar-Lara, M., Cortés-Pérez, I., Díaz-Fernández, Á., Montilla-Ibáñez, M. d. A., Sedeño-Vidal, A., & Obrero-Gaitán, E. (2024). Virtual Reality-Based Therapy Can Enhance Balance and Muscular Endurance in Children and Adolescents with Down Syndrome: A Systematic Review with a Meta-Analysis. Bioengineering, 11(11), 1112. https://doi.org/10.3390/bioengineering11111112

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop