Consequences of Virtual Reality Experience on Biomechanical Gait Parameters in Children with Cerebral Palsy: A Scoping Review

Figures & data

Figure 1. PRISMA flow diagram of the study selection process.

Table 1. Characteristics of studies included in the review. (s)CP=(Spastic) Cerebral Palsy; TD=Typical Development; VR=Virtual Reality; GRAIL=Gait Real-time Analysis Interactive Lab system; GMFCS=Gross Motor Function Classification Scale; EMG=Electromyography; CAREN=Computer-Assisted Rehabilitation Environment system.

Author, year (country)	Study design and main objective	Participants	Baseline walking	Walking conditions	VR-condition	Motion capture system	Biomechanical outcome parameters	Key findings
van der Krogt et al. 2014 (27) (The Netherlands)	Cross-sectional To compare self-paced treadmill walking in a virtual environment to walking in a gait lab and to walking outside the lab in children with CP	9 sCP children (8-14y) - unilateral (n = 2) - bilateral (n = 7) 11 TD children (8-15y) Inclusion criteria CP: Walk independently; GMFCS I/II; no multilevel surgery, selective dorsal rhizotomy or baclofen treatment within last year; no botulinum toxin A treatment previous 16 weeks	Overground walking in a conventional gait lab without VR	Overground walking in a conventional gait lab; self-paced treadmill walking placed in a virtual environment; indoor courtyard to allow for natural walking	Dual-belt instrumented treadmill placed in a speed-matched virtual environment, projected on a semicircular screen, displaying an endless, straight forest road and scenery	GRAIL; Optotrak	Spatiotemporal parameters and kinematics Deviation of kinematics (Gait Profile Score, Movement Analysis Profile)	Reduced walking speed and stride length in overground and VR walking; wider stride width in VR walking; for CP, decreased peak ankle dorsiflex in swing and increased knee flexion at initial contact in VR walking; more deviation in gait patterns in VR walking
Sloot et al. 2015 (28) (The Netherlands)	Cross-sectional To compare the effect of self-paced versus fixed speed treadmill walking and of treadmill walking with and without a VR on gait parameters in children with CP	See van der Krogt et al. 2014 (27)	See van der Krogt et al. 2014 (27)	Treadmill walking at fixed speed and self-paced, both with and without VR	See van der Krogt et al. 2014 (27)	See van der Krogt et al. 2014 (27)	Spatiotemporal parameters, kinematics, and kinetics	Self-paced treadmill walking increased walking speed and stance percentage in CP; VR walking increased absorbed ankle work, increased range of hip extension in CP and decreased between-stride walking speed variability in CP
Lim 2014 (33) (Republic of Korea)	Cross-sectional To compare the effect of slow, normal, and fast optic flow speed on gait parameters in children with CP	10 CP children (3-6y) - unilateral (n = 10) Inclusion criteria CP: Current diagnosis of hemiplegic CP; walk unassisted or with minimal assistance; GMFCS I/II; no visual deficit	Overground walking using GAITRite without visual program input information	Walking across the walkway of the GAITRite system at slow (0.25 times normal speed), normal and fast optic flow speed (2 times normal speed)	Visual information was projected on a screen using a VR software, which mimicked walking in a park; optic flow speed at three different levels: slow, normal, and fast	GAITRite system	Spatiotemporal parameters (affected versus non-affected side)	Fast optic flow speed increased, and slow optic flow speed decreased walking velocity, cadence, step length, base of support, single support
van Gelder et al. 2017 (31) (The Netherlands)	Cross-sectional To determine the effect of real-time visual feedback of kinematics on hip and knee extension in children with CP	16 sCP children (6-16y) 11 TD children (6-16y) Inclusion criteria CP: Gait pattern with excessive knee flexion and/or hip during stance; walk independently; sufficient cognitive ability; no botulinum toxin-A treatment previous 16 weeks; no orthopedic surgery, intrathecal baclofen treatment, selective dorsal rhizotomy previous 12 months	Treadmill walking at self-selected fixed speed for at least 3 minutes with no feedback	Treadmill walking at self-selected fixed speed with no feedback, real-time feedback on knee extension or hip extension (CP: most affected side)	Dual-belt instrumented treadmill with semicircular screen, projecting a visually engaging VR environment including variations of real-time feedback	GRAIL; Vicon	Spatiotemporal parameters and kinematics Deviation of kinematics (Gait Profile Score, Movement Analysis Profile)	Hip extension feedback increased hip and knee extension; knee extension feedback increased knee extension; no effect of feedback on deviations of kinematics
Booth et al. 2019 (29) (The Netherlands)	Repeated measures To explore the effect of avatar-based biofeedback on step length, knee extension and ankle power on gait parameters in children with CP	22 sCP children and related (hereditary) forms of spastic paresis (6-16y) - unilateral (n = 6) - bilateral (n = 16) Inclusion criteria CP: Diagnosis of spastic paresis (unilateral and bilateral); GMFCS I/II; aged 5-16y; no severe cognitive impairment; no botulinum toxin-A treatment previous 6 months; no orthopedic surgery, intrathecal baclofen treatment, selective dorsal rhizotomy previous 12 months	Treadmill walking for 1 min at self-selected comfortable walking speed, without biofeedback, but VR scene visible throughout	Treadmill walking at self-selected, fixed, comfortable walking speed; baseline walking with optic flow, avatar only, biofeedback on knee extension with bar, with avatar, on knee extension with avatar, on step length with avatar, on ankle power with avatar	Dual-belt instrumented treadmill with VR environment projected on a semicircular screen	GRAIL; Bonita 10; Vicon	Spatiotemporal parameters, kinematics, and kinetics Deviation of kinematics (Gait Profile Score)	Biofeedback with avatar only increased hip abduction during swing, maximal hip extension and range of hip and knee; biofeedback on knee extension increased knee extension at initial contact and during stance and step length; biofeedback on ankle power increased peak ankle power and peak hip power during push-off
Booth et al. 2019 (30) (The Netherlands)	Repeated measures To establish the effect of real-time biofeedback on selective motor control, quantified by synergy analysis in children with CP	23 sCP children and related (hereditary) forms of spastic paresis (6-16y) - unilateral (n = 8) - bilateral (n = 15) → same dataset as Booth et al. 2019 (27) 27 TD children (5-16y) Inclusion criteria CP: Diagnosis of spastic paresis (unilateral and bilateral); GMFCS I/II; aged 5-16y; no severe cognitive impairment; no botulinum toxin-A treatment previous 6 months; no orthopedic surgery, intrathecal baclofen treatment, selective dorsal rhizotomy previous 12 months	See Booth et al. 2019 (29)	Treadmill walking at self-selected, fixed, comfortable walking speed; baseline walking, avatar-based biofeedback on step length, knee extension during late swing and ankle push off power	See Booth et al. 2019 (29)	See Booth et al. 2019 (29)	Surface EMG on 8 muscles of the (most affected) lower leg	Biofeedback on ankle power increased the number of muscle synergies; no changes for biofeedback on knee extension or step length
Ma et al. 2019 (32) (China)	Cross-sectional To compare the effects of level versus uphill treadmill walking under a VR environment on gait parameters in children with CP	10 sCP children (6-12y) - Bilateral (n = 10) 10 TD children (7.9 ± 1.4 y) Inclusion criteria CP: Diagnosed with diplegic CP; 6-12y old; GMFCSI/II; capable of understanding and executing instructions; no botulinum toxin lower extremities or surgery previous 6 months Inclusion criteria CP/TD: No severe heart and lung diseases; no visual or auditory system disorders	Level treadmill walking with VR	Level and uphill treadmill walking at self-selected walking speed in the VR environment on a virtual walkway	Split-belt force plate instrumented treadmill with VR environment projected on a semicircular screen	CAREN; Vicon	Spatiotemporal parameters, kinematics, and kinetics	Uphill treadmill walking decreased walking speed, stride length, peak hip abduction moment in CP, and increased stance phase percentage, peak ankle dorsiflexion, knee flexion and peak hip extension moment in CP

Table 2. Risk of bias of the included studies based on the AXIS Critical Appraisal Tool for cross-sectional studies (25). Y=Yes; N=No; ND=not disclosed; NA=not applicable; UC=unclear.

AXIS Critical Appraisal Tool	Booth et al. 2019 (29)	Booth et al. 2019 (30)	Lim 2014 (33)	Ma et al. 2019 (32)	Sloot et al. 2015 (28)	Van der Krogt et al. 2014 (27)	Van Gelder et al. 2017 (31)
Introduction
1. Were the aims/objectives of the study clear?	Y	N	N	Y	Y	Y	Y
Methods
2. Was the study design appropriate for the stated aim(s)?	Y	Y	Y	Y	Y	Y	Y
3. Was the sample size justified?	N	N	N	N	N	N	N
4. Was the target/reference population clearly defined? (Is it clear who the research was about?)	Y	Y	N	N	N	N	Y
5. Was the sample frame taken from an appropriate population base so that it closely represented the target/reference population under investigation?	Y	Y	UC	UC	UC	UC	Y
6. Was the selection process likely to select subjects/participants that were representative of the target/reference population under investigation?	Y	Y	UC	UC	UC	UC	Y
7. Were measures undertaken to address and categorize non-responders?	N	N	N	N	N	N	N
8. Were the risk factor and outcome variables measured appropriate to the aims of the study?	Y	Y	Y	Y	Y	Y	Y
9. Were the risk factor and outcome variables measured correctly using instruments/measurements that had been trialed, piloted or published previously?	Y	Y	Y	Y	Y	Y	Y
10. Is it clear what was used to determined statistical significance and/or precision estimates? (e.g., p values, CIs)	Y	Y	Y	Y	Y	Y	Y
11. Were the methods (including statistical methods) sufficiently described to enable them to be repeated?	Y	Y	N	Y	Y	Y	Y
Results
12. Were the basic data adequately described?	Y	Y	Y	Y	Y	Y	Y
13. Does the response rate raise concerns about non- response bias?	NA	NA	NA	NA	NA	NA	NA
14. If appropriate, was information about non- responders described?	N	N	N	N	N	N	N
15. Were the results internally consistent?	Y	Y	N	Y	Y	Y	Y
16. Were the results for the analyses described in the methods, presented?	Y	Y	N	Y	Y	Y	Y
Discussion
17. Were the authors’ discussions and conclusions justified by the results?	Y	Y	Y	Y	Y	Y	Y
18. Were the limitations of the study discussed?	Y	Y	Y	Y	N	Y	N
Others
19. Were there any funding sources or conflicts of interest that may affect the authors’ interpretation of the results?	N	N	ND	N	N	N	N
20. Was ethical approval or consent of participants attained?	Y	Y	Y	Y	Y	Y	Y

Table 3. Risk of bias of the included studies based on the Joanna Briggs Institute (JBI) checklist for analytical cross-sectional studies (26). Y=Yes; N=No; NA=Not applicable.

Joanna Briggs Institute (JBI) Checklist	Booth et al. 2019 (29)	Booth et al. 2019 (30)	Lim 2014 (33)	Ma et al. 2019 (32)	Sloot et al. 2015 (28)	Van der Krogt et al. 2014 (27)	Van Gelder et al. 2017 (31)
1. Were the criteria for inclusion in the sample clearly defined?	Y	Y	N	Y	Y	Y	Y
2. Were the study subjects and the setting described in detail?	Y	Y	N	N	N	N	Y
3. Was the exposure measured in a valid and reliable way?	Y	Y	Y	Y	Y	Y	Y
4. Were objective, standard criteria used for measurement of the condition?	N	N	N	N	N	N	N
5. Were confounding factors identified?	N	N	N	N	Y	N	N
6. Were strategies to deal with confounding factors stated?	NA	NA	NA	NA	Y	NA	NA
7. Were the outcomes measured in a valid and reliable way?	Y	Y	Y	Y	Y	Y	Y
8. Was appropriate statistical analysis used?	Y	Y	Y	Y	Y	Y	Y

Table 4. Biomechanical gait parameters measured in the included studies during virtual reality exposure. Parameters highlighted in yellow were reported in 3 studies, in orange in 4 or more studies. COM=Center of Mass; COP=Center of Pressure; IC=Initial Contact; LR=Loading Response.

Table A1. Search terms used for the review. tiab=Title/Abstract; ti=Title; ab=Abstract; kw=Keyword; TS=Topic Search.

Database	Population	Exposure	Outcome	NOT
MEDLINE	(“Cerebral Palsy”[Mesh] OR “Hemiplegia”[Mesh] OR “Paraplegia”[Mesh] OR “Quadriplegia”[Mesh] OR “Paresis”[Mesh] OR “Paraparesis, Spastic”[Mesh] OR “Neurodevelopmental Disorders”[Mesh:NoExp] OR “Gait Disorders, Neurologic”[Mesh] OR “cerebral pals*”[tiab] OR “little disease*”[tiab] OR “little’s disease*”[tiab] OR dipleg*[tiab] OR monopleg*[tiab] OR hemipleg*[tiab] OR spastic*[tiab] OR quadripleg*[tiab] OR parapleg*[tiab] OR hemipares*[tiab] OR pares*[tiab] OR neurodevelop*[tiab])	(“Virtual Reality”[Mesh] OR “Virtual Reality Exposure Therapy”[Mesh] OR “Simulation Training”[Mesh] OR “Augmented Reality”[Mesh] OR “Video Games”[Mesh] OR “User-Computer Interface”[Mesh] OR “virtual real*”[tiab] OR “virtual environment*”[tiab] OR immers*[tiab] OR simulat*[tiab] OR “3-D environment*”[tiab] OR computer*[tiab] OR artificial*[tiab] OR illusion*[tiab] OR “video gam*”[tiab] OR “augmented real*”[tiab] OR “mediated real*”[tiab] OR “multimediated real*”[tiab] OR “extended real*”[tiab] OR “hybrid real*”[tiab] OR “mixed real*”[tiab] OR “mix real*”[tiab] OR virtualit*[tiab] OR cyber*[tiab] OR Kinect*[tiab] OR Wii*[tiab] OR Playstation*[tiab] OR “Play Station*”[tiab] OR “user-computer interface*”[tiab] OR biofeedback*[tiab])	(“Gait Analysis”[Mesh] OR “Gait”[Mesh] OR “Biomechanical Phenomena”[Mesh] OR “Spatio-Temporal Analysis”[Mesh] OR “Locomotion”[Mesh] OR “Standing Position”[Mesh] OR “Walking”[Mesh] OR “Proprioception”[Mesh] OR “Postural Balance”[Mesh] OR “motion analys*”[tiab] OR gait*[tiab] OR walk*[tiab] OR stand*[tiab] OR stance*[tiab] OR locomot*[tiab] OR kinematic*[tiab] OR kinetic*[tiab] OR biomechanic*[tiab] OR spatiotemporal*[tiab] OR spatio-temporal*[tiab] OR “ground reaction force*”[tiab] OR “center of mass*”[tiab] OR “center of pressure*”[tiab] OR balance*[tiab] OR equilib*[tiab] OR coordinat*[tiab] OR propriocept*[tiab])	(“animals”[Mesh] NOT “humans”[Mesh])
Embase	(“Cerebral Palsy”/exp OR “Hemiplegia”/exp OR “Paraplegia”/exp OR “Quadriplegia”/exp OR “Paresis”/exp OR “Spastic Paraplegia”/exp OR “Neurodevelopmental Disease”/exp OR “Neurodevelopmental disability”/exp OR “Neurologic Gait Disorder”/exp OR “Little Disease”/exp OR “cerebral pals*”:ti,ab,kw OR “little disease*”:ti,ab,kw OR dipleg*:ti,ab,kw OR monopleg*:ti,ab,kw OR hemipleg*:ti,ab,kw OR spastic*:ti,ab,kw OR quadripleg*:ti,ab,kw OR parapleg*:ti,ab,kw OR hemipares*:ti,ab,kw OR pares*:ti,ab,kw OR neurodevelop*:ti,ab,kw)	(“Virtual Reality”/exp OR “Virtual Reality Exposure Therapy”/exp OR “Virtual Reality System”/exp OR “Augmented Reality”/exp OR “Augmented Reality System”/exp OR “Video Game”/exp OR “Computer Interface”/exp OR “Nintendo Wii”/exp OR “Biofeedback”/exp OR ‘virtual real*:”ti,ab,kw OR ‘virtual environment*:’ti,ab,kw OR immers*:ti,ab,kw OR simulat*:ti,ab,kw OR ”3-D environment*:’ti,ab,kw OR computer*:ti,ab,kw OR artificial*:ti,ab,kw OR illusion*:ti,ab,kw OR “video gam*:”ti,ab,kw OR “augmented real*:”ti,ab,kw OR “mediated real*:”ti,ab,kw OR “multimediated real*:”ti,ab,kw OR “extended real*:”ti,ab,kw OR “hybrid real*:”ti,ab,kw OR “mixed real*:”ti,ab,kw OR “mix real*:”ti,ab,kw OR virtualit*:ti,ab,kw OR cyber*:ti,ab,kw OR Kinect*:ti,ab,kw OR Wii*:ti,ab,kw OR Playstation*:ti,ab,kw OR “Play Station*:”ti,ab,kw OR “user-computer interface*:”ti,ab,kw OR biofeedback*:ti,ab,kw)	(“Gait Analysis System”/exp OR “Gait”/exp OR “Motion Analysis”/exp OR “Motion Analysis System”/exp OR “Biomechanics”/exp OR “Biomechanical Software”/exp OR “Spatiotemporal Analysis”/exp OR “Locomotion”/exp OR “Standing”/exp OR “Standing Balance”/exp OR “Walking”/exp OR “Proprioception”/exp OR “Proprioceptive Feedback”/exp OR “Postural Control”/exp OR “Body Equilibrium”/exp OR “motion analys*”:ti,ab,kw OR gait*:ti,ab,kw OR walk*:ti,ab,kw OR stand*:ti,ab,kw OR stance*:ti,ab,kw OR locomot*:ti,ab,kw OR kinematic*:ti,ab,kw OR kinetic*:ti,ab,kw OR biomechanic*:ti,ab,kw OR spatiotemporal*:ti,ab,kw OR spatio-temporal*:ti,ab,kw OR “ground reaction force*”:ti,ab,kw OR “center of mass*”:ti,ab,kw OR “center of pressure*”:ti,ab,kw OR balance*:ti,ab,kw OR equilib*:ti,ab,kw OR coordinat*:ti,ab,kw OR propriocept*:ti,ab,kw)	((“animal”/exp OR “animal experiment”/exp OR “nonhuman”/exp) NOT (“human”/exp OR “human experiment”/exp))
Web of Science	(TS=(“cerebral pals*”) OR TS=(hemipleg*) OR TS=(parapleg*) OR TS=(quadripleg*) OR TS=(parapleg*) OR TS=(dipleg*) OR TS=(monopleg*) OR TS=(pares*) OR TS=(hemipares*) OR TS=(spastic*) OR TS=(neurodevelop*) OR TS=(“little disease*”) OR TS=(“little’s disease*”))	(TS=(“virtual real*”) OR TS=(“augmented real*”) OR TS=(“mediated real*”) OR TS=(“multimediated real*”) OR TS=(“extended real*”) OR TS=(“hybrid real*”) OR TS=(“mixed real*”) OR TS=(“mix real*”) OR TS=(virtualit*) OR TS=(“video gam*”) OR TS=(biofeedback*) OR TS=(“virtual environment*”) OR TS=(immers*) OR TS=(simulat*) OR TS=(“3-D environment*”) OR TS=(computer*) OR TS=(artificial*) OR TS=(illusion*) OR TS=(cyber*) OR TS=(Kinect*) OR TS=(Wii*) OR TS=(Playstation*) OR TS=(“Play Station*”) OR TS=(“user-computer interface*”))	(TS=(“gait analys*”) OR TS=(gait) OR TS=(“motion analys*”) OR TS=(biomechanic*) OR TS=(spatiotemp*) OR TS=(“spatio-temp*”) OR TS=(locomot*) OR TS=(standing*) OR TS=(balance) OR TS=(walk*) OR TS=(stand*) OR TS=(stance*) OR TS=(propriocept*) OR TS=(postural) OR TS=(equilib*) OR TS=(kinematic*) OR TS=(kinetic*) OR TS=(“ground reaction force*”) OR TS=(“center of mass”) OR TS=(“center of pressure”) OR TS=(coordinat*))	-