Keywords
traumatic brain injury - virtual reality - rehabilitation - Montreal cognitive assessment
- cognitive function
Introduction
Traumatic brain injury (TBI) is a medical condition that causes brain damage after
receiving an external, powerful, and violent head injury (such as a fall from a height,
a sports injury, or a car accident) or having an object to penetrate the skull (i.e.,
bullets). TBI causes the majority of long-term disabilities and fatalities in young
adults, and it is a major socioeconomic and healthcare burden.[1]
[2] Priority should be given to managing TBI patients through an integrated, tailored,
thorough diagnostic, treatment, and rehabilitation program. Following a TBI, behavioral
alterations and aberrant cognitive function are caused by modifications of neurotransmitter
and neuroendocrine activity.[3] Executive function, problem-solving, memory, and attention are just a few of the
cognitive problems that a TBI can lead to. Impaired daily living activities are regarded
as executive function impairment, which is a predictive marker for rehabilitative
activities. There is a shortage of comprehensive rehabilitation services in many developing
nations, including India, as well as a lack of knowledge about rehabilitation and
its solutions. This makes it more difficult for post-TBI survivors to work and stresses
out carers. To improve both quality of life and cognitive performance after a TBI,
rehabilitation is essential.
Many studies have shown the potential efficiency of cutting-edge methods, such as
virtual reality (VR), during the various phases of rehabilitation following a TBI.[4]
[5]
[6] A computer-based solution known as VR produces artificial settings with special
sensory stimuli that may be interacted with in real time.[7] VR can be nonimmersive, where virtual content is displayed on a computer screen
using conventional interfaces, or immersive, where virtual content is typically displayed
by a head-mounted display (giving the user the impression that he or she has entered
the computer-generated artificial world). Finding items and performing tasks in VR
can mimic the ecological needs of the real world, which can enhance the brain's capacity
for plasticity and regeneration processes.[6] VR has been demonstrated to boost cognitive functions in TBI patients as a rehabilitation
technique. Moreover, it increases motivation and enjoyment, two crucial elements for
effective rehabilitation exercise and adherence.[8] In short, VR offers a fun, interactive environment that can improve patient compliance
and the effectiveness of rehabilitation itself. It can also be tailored to the specific
needs of the patient.
This study was conducted to evaluate the role of VR rehabilitation in cognitive assessment
and rehabilitation in individuals affected by TBI and to observe whether the benefits
of in-patient VR rehabilitation are sustainable by assessing the patients in follow-up
examination a minimum after 1 month of discharge.
Materials and Methods
After obtaining institutional ethical committee approval, this randomized prospective
comparative study was conducted from July 1, 2021, to December 31, 2022. The patients
were enrolled in the study after obtaining informed and written consent. No extra
financial burden would be incurred for the patient.
A total 80 patients with TBI after obtaining written and informed consent were enrolled
in study. Patients with following characteristics were included: Aged between 18 and
60 years, ability to sit for at least 15 minutes (Including at least 1 minute without
support), presence of mild-to-moderate cognitive impairment (Montreal Cognitive Assessment
[MOCA] from 10 to 26). Patients with global aphasia, poor comprehension, and comorbidities
interfering with rehabilitation, known case of psychiatric or central nervous system
pathology or medical and surgical disease that interfere with the study and patient
with multiple injuries that interfere with the uses of VR user interface were excluded
from the study.
The rehabilitation program was started on patients with a history of TBI after completing
the initial clinical assessment within 48 hours of admission. After obtaining their
written informed consent, all patients were evaluated with detailed clinical examination,
and sociodemographic, educational, current neurological and radiological and biochemical
data were recorded. Assessment of motor, cognitive and functional outcomes was done
at three points: prior training, after 15 days, and after 1 month (follow-up).
All patients were divided into case and control groups randomly; the control group
received standard care that includes antiepileptics, analgesics, and physiotherapy
focused to improve locomotion, spasticity reduction, balance improvement, positioning,
resistive, and stretching exercises and graded gait training and for tic-tac-toe,
matchmaking and Sudoku like exercises for cognitive rehabilitation. At the time of
discharge, these patients were advised home-based program and asked to report for
follow-up after 15 and 30 days from the date of TBI.
All patients in the case group received standard care similar to the control group
along with intensive VR training sessions once a day for 6 days a week; first session
was conducted after 2 days of admission. Each VR session was a one-on-one session,
using the patient-centered approach with the level of individual task difficulty varied
according to the participant's level of performance; each session was conducted with
a registered clinician
There were three different VR exercises and each exercise had 10 difficulty levels
and it scores were according to patient performance ranging from 1 to 3 stars. If
the patient got 2 or more than 2 stars, then only he proceeded to the next level;
otherwise he shifted to another exercise for that particular VR session.
Outcome Measures
Each participant was assessed using neuropsychological evaluation before the training,
at the time of discharge and during the follow-up by using the MOCA and a group of
tests that include the Tower of London (TOL) test, trail-making test, and go and no
go test to assess cognitive function.
-
1)
Montreal Cognitive Assessment: MOCA was a screening tool for cognition and is found to be more sensitive and specific
for the detection of mild cognitive deficits compared with Folstein mini–mental state
examination.[9] MOCA tests visuospatial executive, naming, memory, attention, language, abstraction,
delayed recall and orientation aspects of cognition. The total MOCA score was calculated
by summing the score of all domains from 0 to 30. Scores less than 10 indicate severe,
10 to 17 moderate, and scores between 18 and 26 suggestive of mild impairment. A score
more than 26 is interpreted as normal cognition.
Patient with MOCA score ranging from 10 to 26 was included in the study and was further
assessed by a group of quantitative cognitive and functional assessment tests that
include the TOL test and trail-making test; these group of tests will be done by another
clinician to reduce the bias.
-
2)
Tower of London test: The TOL was a test used for the assessment of executive functioning specifically
to detect deficits in planning.[10]
[11] The TOL test includes transferring three-colored disks between three vertical rods,
from an initial position to a prespecified goal arrangement. Solving the TOL problem
within a limited number of moves requires planning the sequence of action before starting
to move the discs. It is, therefore, considered a planning test.
-
3)
Trail-making test: This test can provide information about visual search speed, scanning, speed of processing,
mental flexibility, as well as executive functioning.[12] Trail-making requires a subject to connect a sequence of 25 consecutive targets
on a sheet of paper or computer screen.
Data Analysis
Numerical variables were summarized as mean and standard deviation and were analyzed
by using various parametric tests. Nominal/categorical variables were presented as
proportions and were analyzed using the chi-squared test and other suitable nonsuitable,
nonparametric tests.
p-Value less than 0.05 would be considered statistically significant.
Results
Sociodemographic characteristics of study population: In [Table 1], the mean age of cases was 49.73 years, and the mean age of control was 56.17 years.
Both in cases and control, there was male preponderance. Their education level shows
no significant difference.
Table 1
Sociodemographic characteristics of study population
|
Characteristic
|
Case
|
Control
|
p-Value
|
|
Total n
|
40
|
40
|
–
|
|
Age, years (mean)
|
49.73 (9.05)
|
56.5 (7.13)
|
0.43
|
|
Male (%)
|
28
|
27
|
0.9
|
|
Female
|
22
|
23
|
|
Education
|
|
Up to primary (1–5th)
|
12
|
14
|
0.71
|
|
Up to Sr. secondary (6–12th)
|
9
|
7
|
|
Graduation
|
8
|
5
|
|
Professional
|
5
|
5
|
|
Home maker
|
6
|
9
|
Clinical characteristics of study population: As described in [Table 2], our study showed maximum prevalence of mild injury, followed by moderate and then
severe. Among cases, the major reason behind TBI was a fall in 21 patients, while
among controls, the reason was motor vehicle accidents in 22 cases. Time since trauma
in both cases and control had no significant difference; mean time since trauma was
approximately 7 hours. In both groups, the lesion was more common on the left side
of cerebral hemisphere.
Table 2
Clinical characteristics of study population
|
Characteristic
|
Case
|
Control
|
p-Value
|
|
Total, n
|
40
|
40
|
–
|
|
Injury Severity
|
|
|
0.37
|
|
Mild (%)
|
25
|
13
|
|
|
Moderate (%)
|
10
|
25
|
|
|
Severe (%)
|
5
|
2
|
|
|
Mode of injury
|
|
|
0.61
|
|
Falls
|
19
|
18
|
|
|
Motor vehicle accident
|
21
|
22
|
|
|
Time since trauma (in hours)
|
7.1 ± 6.7
|
7.25 ± 6.8
|
0.917
|
|
Lesion site
|
|
|
0.84
|
|
Right
|
11
|
13
|
|
Left
|
29
|
27
|
Cognitive and functional score (MOCA, TOL and TMT) in patient with TBI: In [Table 3], it is observed that variables MoCA, TOL, and TMT represented significant differences
after VR sessions, while in the control group, there is no significant difference.
Table 3
Cognitive and functional score (MOCA, TOL, and TMT) in patient with traumatic brain
injury
|
Variables
|
Groups
|
Mean value on admission
|
Mean value at discharge
|
Mean values at follow-up
|
Degree of freedom
|
p-Value
|
|
MoCA
|
Case
|
16.5
|
24.3
|
28.5
|
1
|
< 0.001
|
|
Control
|
17
|
19
|
21
|
1
|
0.081
|
|
TOL
|
Case
|
11.75
|
22
|
32.5
|
1
|
< 0.001
|
|
Control
|
10
|
13
|
15
|
1
|
0.061
|
|
TMT
|
Case
|
14.05 s
|
27.5 s
|
42.07 s
|
1
|
< 0.001
|
|
Control
|
13 s
|
17 s
|
19 s
|
1
|
0.068
|
Abbreviations: MoCA, Montreal Cognitive Assessment; TMT, Trail Making Test; TOL, Tower
of London.
Cognitive domain score using MOCA scale:
[Table 4] describes therapeutic use of VR had positive and significant effects on cognitive
function in individuals; there was a significant improvement in the subcategories
such as global cognition, executive function, language, abstraction, recall, orientation,
and attention when compared with the control group.
Table 4
Cognitive domain score using MoCA scale
|
Cognitive subdomains
|
Descriptive statistics
|
Admission
|
Discharge
|
Follow-up
|
p-Value
|
|
Visuospatial/Executive
|
Case
|
0.5 ± 0.23
|
0.81 ± 0.15
|
0.96 ± 0.08
|
0.041
|
|
Control
|
0.48 ± 0.18
|
0.51 ± 0.09
|
0.59 ± 0.08
|
0.82
|
|
Naming
|
Case
|
0.64 ± 0.14
|
0.7 ± 0.16
|
0.84 ± 0.08
|
0.002
|
|
Control
|
0.63 ± 0.09
|
0.64 ± 0.12
|
0.65 ± 0.01
|
0.72
|
|
Attention
|
Case
|
0.76 ± 0.19
|
0.77 ± 0.15
|
0.99 ± 0.03
|
0.004
|
|
Control
|
0.75 ± 0.18
|
0.75 ± 0.12
|
0.78 ± 0.15
|
0.91
|
|
Language
|
Case
|
0.65 ± 0.13
|
0.68 ± 0.15
|
0.84 ± 0.05
|
0.048
|
|
Control
|
0.62 ± 0.14
|
0.64 ± 0.14
|
0.71 ± 0.16
|
0.062
|
|
Abstraction
|
Case
|
0.68 ± 0.18
|
0.71 ± 0.19
|
0.82 ± 0.21
|
0.001
|
|
Control
|
0.67 ± 0.14
|
0.64 ± 0.12
|
0.68 ± 0.16
|
0.92
|
|
Delayed recall
|
Case
|
0.71 ± 0.21
|
0.75 ± 0.24
|
0.81 ± 0.26
|
0.037
|
|
Control
|
0.69 ± 0.14
|
0.71 ± 0.14
|
0.71 ± 0.16
|
0.91
|
|
Orientation
|
Case
|
0.72 ± 0.19
|
0.75 ± 0.21
|
0.81 ± 0.23
|
0.048
|
|
Control
|
0.70 ± 0.18
|
0.71 ± 0.18
|
0.73 ± 0.20
|
0.82
|
Abbreviation: MoCA, Montreal Cognitive Assessment.
Discussion
Current literature demonstrates that VR could be useful as a rehabilitation tool in
cognitive recovery post-TBI. However, the evaluation protocols with VR have been mainly
applied in mild TBI, which is difficult to evaluate with traditional tools. Instead,
VR treatment protocols for cognitive rehabilitation are most widely used (i.e., from
mild-to-severe conditions), although the efficacy of these interventions should be
further explored indeed, although studies suggest that VR training can provide innovative
treatment options for TBI. Hence, the study[13] was conducted to evaluate the role of VR rehabilitation in cognitive assessment
and rehabilitation in individuals affected by TBI.
In our study, the mean age of cases was 49.73 years, and the mean age of control was
56.17 years. Both in cases and control, there was male preponderance. Their education
level shows no significant difference. Similarly, a study by Lui et al showed more
males were admitted acutely for TBI, which was consistent with other demographic studies,
as male sex has been established as a risk factor for TBI.[14]
[15] The suggested reasons for higher TBI risk in males were related to males often participating
in more risk-taking behavior, contact sports, and alcohol consumption.[16]
Similarly, a study by Liew et al[17] showed a peak incidence of TBI in elderly patients, especially those aged between
45 and 60 years, with falls being the predominant mechanism of TBI in the elderly,
whereas road traffic accident was the leading cause in younger patients. This was
also the case in a recent study by Liew et al that reported a shift in local TBI demographics
toward an older population, with an increased incidence of falls.
The severity of injury in our study showed maximum prevalence of mild injury, followed
by moderate and then severe. Among cases, the major reason behind TBI was motor vehicle
accidents in 21 patients, while among controls, the reason was motor vehicle accidents
in 22 cases. Time since trauma in both cases and control had no significant difference;
mean time since trauma was approximately 7 hours. In both groups, the lesion was more
common on the left side.
Similar results were observed in articles of Hanson et al[18], Ponsky et al,[19] and Macpherson et al[20] where motor vehicle collision are common mechanisms of TBI.
Similar data of severity were stated by McMahon et al,[21] where the majority of patients selected for VR were older patients with mild TBI.
Functional impairment is prevalent in mild TBI, and studies have shown that mild TBI
can result in cognitive and psychosocial impairment. Older patients with mild TBI
have an increased risk of poor cognitive performance, which could explain their need
for inpatient rehabilitation, despite the mild severity.
In our study, all patients in the case group received standard care similar to the
control group along with intensive VR training sessions once a day for 6 days a week;
first session was conducted after 2 days of admission. Each VR session had a one-on-one
session, using a patient-centered approach with the level of individual task difficulty
varied according to the participant's level of performance each session was conducted
with a registered clinician. Virtual rehabilitation will be conducted in a private
room at the hospital, free of distraction using handheld objects, the participant
engaged in a virtual environment presented on an LCD screen with a built CPU by using
a Tyro motion machine. The patient will interact with virtual scenarios and audiovisual
stimuli, creating a multiple sensory involvement that facilitates attention, visual–spatial,
memory, and executive skills. There were three different VR exercises and each exercise
had 10 difficulty levels and it scored according to the patient, ranging from 1 to
3 stars.
There were several tools for VR in other studies that can be used with different costs
and complexity. Currently, studies with VR use advanced and complex instruments. An
example in the CAREN used by Onakomaiya et al.[22] In a study of Levy et al,[23] a VR grocery store was used as an assessment and intervention tool. However, in
the study of Besnard et al[24], a nonimmersive virtual coffee task—a virtual kitchen to assess daily-life activities,
was used. In a study of Canty et al,[25] prospective memory task (i.e., the VR shopping task) was used, whereas Larson et
al used VR[26] and robotics technology.
In our study, it is observed that variables MoCA, TOL, and TMT represented significant
differences after VR sessions, while in the control group, there is no significant
difference. Therapeutic use of VR had positive and significant effects on cognitive
function in individuals;, there was a significant improvement in the subcategories
such as global cognition, executive function, language, abstraction, recall, orientation,
and attention when compared with the control group.
Similarly, in study of Kim et al,[27] there was significant improvement in the subcategories such as global cognition
(mean difference [MD] = −1.15, 95% confidence interval [CI]: −2.83 to 0.53), executive
function (MD = −2.56, 95% CI: −8.94 to 3.82), working memory (MD = 0.08, 95% CI: −0.93
to 1.10), memory function (MD = −0.26, 95% CI: −0.73 to 0.22), and attention (MD = −0.61,
95% CI: −1.26 to 0.05) when compared with the control group. Our results are also
similar to the results, reported in previous meta-analyses of Kim et al and Yu et
al[28], which showed significant improvements in global cognition after VR. A previous
meta-analysis by Zhu et al[29] showed significant improvements in executive function and memory function. However,
another meta-analysis by Wu et al[30] and Zhong et al[31] reported no positive effects on memory function, execution function, and attention
after VR.
Similar results were observed in the systemic review of Shin and Kim[32] where the types of VR programs that have been used in cognitive evaluations of patients
with brain injury were identified and studies of cognitive interventions were reviewed
according to PICO methods. In the included studies, the VR programs could distinguish
the cognitive disability of patients in comparison with healthy subjects. Thus, VR
could be used as a new assessment method of the cognitive function of patients with
brain injury.
Hence, in this study, the therapeutic application of VR in individuals with TBI was
more effective in improving cognitive function when compared with the control group;
subcategories of cognitive function also showed significant improvement.
Conclusion
Therefore, by seeing the results from the following charts and tables as depicted
above, we can say that in this study, the therapeutic application of VR in individuals
with TBI was more effective in improving cognitive function when compared with the
control group.
Limitations
Assessment of cognitive and functional outcomes was done at three points: prior training;
after 15 days, and after 1 month (follow-up). However, we were not able to analyze
the efficacy of a particular program in improving cognition. Study with larger sample
size and with longer follow up is necessary.