Non-immersive Virtual Reality Rehabilitation Applied to a Task-oriented Approach for Stroke Patients: A Randomized Controlled Trial

Abstract

Background:

Virtual reality (VR) training allows the creation of the most applicable practice environment incorporated into computer-generated multisensory imagery.

Objectives:

The purpose of this study was to investigate the effects of a virtual training program based on a RAPAEL smart glove on the upper extremity function and quality of life of community-dwelling individuals with chronic hemiparetic stroke.

Methods:

Thirty-six outpatients diagnosed as having a first stroke were selected to receive a therapeutic rehabilitation program at local rehabilitation units. Participants were allocated randomly into two groups: the non-immersive VR training (intervention) group and the recreational activity (control) group. The intervention group received non-immersive VR training using a RAPAEL smart glove for 30 minutes per session, 3 days a week for 8 weeks. The control group performed recreational activities for the same period and also participated in a conventional rehabilitation program for 30 minutes per session, 3 days a week for 8 weeks as an additional therapy. To analyze the effects of the non-immersive VR intervention on upper extremity function, four clinical measures, namely the box and block test (BBT), the Wolf motor function test (WMFT), the Jebsen-Taylor hand function test (JTT), and a grip strength test, were used in this study. For the secondary clinical outcome, the trail-making test (TMT) was used to determine any improvement in cognitive function.

Results:

At week 8, upon completion of the non-immersive VR-training the intervention group demonstrated significantly greater WMFT scores (73.0±12.9 to 81.6±7.5), BBT scores (27.3±8.9 to 34.2±7.1), and grip strength (19.2±8.2 to 23.8±8.5) compared with WMFT scores (70.4±12.1 to 73.2±13.1), BBT scores (27.1±10.5 to 28.8±12.9), and grip strength (18.4±4.2 to 18.3±4.9) in the control group.

Conclusions:

This study suggests that virtual upper extremity training using the RAPAEL smart glove has reasonable and beneficial effects on upper extremity and cognitive function for chronic hemiparetic stroke survivors.

Keywords

Stroke Virtual reality Upper extremity

1 Introduction

Stroke is the leading cause of permanent physical and/or cognitive dysfunction in adults. Most post-stroke patients manifest complex clinical symptoms such as paralysis, unilateral neglect, apraxia, sensory deficit, memory defect, and aphasia (O’Sullivan, Schmitz, & Fulk, 2014). One of the most important issues in stroke rehabilitation is to improve upper extremity dysfunction in order to attain independent community-living and performance of daily activities (Umphred, 2013). To recover from the various symptoms and disabilities through nerve adaptation, therapeutic interventions must be specific, task-oriented, repetitious, spaced in time, progressive in difficulty, and salient to the outcomes targeted (Umphred, 2013).

Previous studies have reported that a task-oriented approach is a component of current therapeutic interventions in stroke rehabilitation (Almhdawi et al., 2016; Ballester, et al., 2016; French et al., 2016). The task-oriented approach may show beneficial effects due to facilitative exercises combined with high repetitive rates (O’Sullivan, Schmitz, & Fulk, 2014). However, with this approach, the motivation of participants is difficult to maintain during the many repetitions of the same upper extremity exercise. The loss of motivation is another barrier that hinders stroke patients from participating in repetitive rehabilitative training (Esfahlani et al., 2018). Virtual reality (VR) training is one of the most effective approaches that is able to maintain the motivation of participants at every training session. VR was initially used for phobias and post-traumatic stress and recently has been used effectively in the field of rehabilitation (Laver et al., 2015).

VR technology allows the creation of the most applicable practice environment incorporated into computer-generated multisensory imagery. VR, in which participants intentionally move to use interactive simulations created with a computer device and a software program, allows patients to engage in an environment that feels as if the objects and events they are seeing are real (Selzer, 2006). Thus, VR training can be incorporated into a VR motor learning program that is applicable to the real-world environment. VR training is divided into immersive and non-immersive training, depending on whether the participant’s environmental center is ego- or exocentric (Huang et al., 2019; Saposnik et al., 2016; Tornbom & Dabielsson, 2018). To generate the virtual environment, the latter used Microsoft’s Xbox and Nintendo Wii technology on a desktop or wide-screen platform and the former used a head mounted display such as the Oculus Rift, Google Cardboard, and/or Samsung Gear VR (Gauthier et al., 2017; Huang et al., 2019; Hung et al., 2019; Mirelman et al., 2016; Triandafilou et al., 2018; Turolla et al., 2018; Yeh et al., 2017).

Non-immersive VR training may be considered a simple, low-cost, high-intensity, task-oriented, patient-centered, community-based therapy for optimizing motor function recovery. Moreover, it can manipulate the training environment to systematically overcome disturbances and environmental constraints to the participant’s movements while minimizing the risk (Saposnik et al., 2016; Teasell et al., 2014). The existing evidence is inadequate to support the applicability and effectiveness of non-immersive VR training based on a desktop or wide-screen platform for improving the upper extremity function of outpatients with chronic hemiparetic stroke. This study evaluated the applicability and effectiveness of non-immersive VR training for improving upper extremity function by using a desktop platform technology in an outpatient rehabilitation program in individuals with chronic hemiparetic stroke.

We conducted a multicenter, single-blinded, randomized controlled trial to compare the effect of non-immersive VR training based on the RAPAEL smart glove with that of recreational therapy based on a computer game program on the motor recovery of the upper extremities. In addition, this study proposes that non-immersive VR training can optimally promote the rehabilitation of the paretic upper limbs and induce functional regains for chronic hemiparetic stroke patients. This study hypothesized that non-immersive VR training may be beneficial for paretic upper limb functioning in chronic hemiparetic stroke patients.

2 Methods

This study was a single-blind, control group, randomized controlled trial conducted at three local rehabilitation centers from 10 October 2018 to 30 April 2019. Ethics Committee approval was obtained from the domain-specific Review Board, Gwangju Women’s University (IRB No. 1041485-201809-HR-001-34). Participants provided informed consent prior to enrolling in this study. Data collection before and after this study was performed by two occupational therapists who were blinded to the study protocol.

2.1 Participants

Thirty-six participants as having a first stroke were included in this study. The participants, aged 55–83 years, had a first stroke confirmed by neuroimaging (CT or MRI) in the 6 months before the start of the study and/or after study enrolment and had mild spasticity (defined as modified Ashworth scale score of < 2 in any of the shoulder, elbow, or wrist/finger muscles). Potential participants were excluded if they had moderate-to-severe cognitive impairment (defined as a mini-mental state examination score of < 19), unilateral neglect, recurrent stroke, inability to follow instructions, uncontrolled hypertension, experienced unstable angina or myocardial infarction within 6 months before the start of the study. Those who participated in another clinical trial that would affect the study results and those with any diagnosis of psychiatric disorders were excluded.

2.2 Randomization and blinding

Participants were randomly assigned to two different training groups: an intervention group (non-immersive VR training using the RAPAEL smart glove, NEOFECT Co., Yung-in, Republic of Korea) and or a control group (recreational activities by computer-generated assignment) by permuted blocks assigned remotely via the internet. Participants did not previously know how to use the training program. To ensure that other caregivers and/or clinicians did not know about their assignments, all study interventions were facilitated by dedicated assessment staff who had no involvement in this study. Baseline and post-intervention assessments were performed by training outcome assessors who were blinded to participant’s training group allocation.

2.3 Study procedures

All participants in the intervention and control groups received the same intensity and duration of non-immersive VR training or recreational activity. This consisted of 24 sessions, a 30-min intensive program per session, 3 days per week for an 8-week period and the conventional rehabilitation program consisted of a 30-min per session activity, 3 days per week for 8 weeks. Participants were assessed at baseline and post-intervention within their outpatient stroke rehabilitation centers by the training outcome assessors. Table 1 illustrates the study procedures.

Table 1
Demographic of the participants (N = 36)

Variables Frequency/mean±SD χ²/p

Intervention group (n = 18) Control group (n = 18)

Age (years) 72.1±5.0 73.2±6.1 0.594

Sex (male/female) 14/4 13/5 1.000

Time since diagnosis (months) 14.8±15.0 15.5±15.0 0.886

Etiology (infarction/hemorrhage) 12/6 12/6 1.000

Paretic side (right/left) 8/10 10/8 0.740

Mini-mental state examination (score) 24.6±3.6 25.6±3.1 0.413

Height (cm) 165.3±8.5 164.8±8.2 0.858

Weight (kg) 70.2±12.3 69.0±11.6 0.772

Box and block test (scores) 27.3±8.9 27.1±10.5 0.946

Grip strength test (kg) 19.2±8.2 18.4±4.2 0.742

Jebsen-Taylor hand function test (scores) 56.2±28.7 55.6±26.7 0.948

Trail marking test (sec) 42.9±16.6 43.0±13.9 0.975

Wolf motor function test (score) 73.0±12.9 70.3±12.1 0.535

Variables	Frequency/mean±SD	χ²/p
Age (years)	72.1±5.0	73.2±6.1	0.594
Sex (male/female)	14/4	13/5	1.000
Time since diagnosis (months)	14.8±15.0	15.5±15.0	0.886
Etiology (infarction/hemorrhage)	12/6	12/6	1.000
Paretic side (right/left)	8/10	10/8	0.740
Mini-mental state examination (score)	24.6±3.6	25.6±3.1	0.413
Height (cm)	165.3±8.5	164.8±8.2	0.858
Weight (kg)	70.2±12.3	69.0±11.6	0.772
Box and block test (scores)	27.3±8.9	27.1±10.5	0.946
Grip strength test (kg)	19.2±8.2	18.4±4.2	0.742
Jebsen-Taylor hand function test (scores)	56.2±28.7	55.6±26.7	0.948
Trail marking test (sec)	42.9±16.6	43.0±13.9	0.975
Wolf motor function test (score)	73.0±12.9	70.3±12.1	0.535

SD, standard deviation

2.4 Therapeutic equipment

This study used the RAPAEL smart rehabilitation solution (consisting of a smart glove as a wireless and real-time biofeedback device) as a non-immersive VR training tool to improve upper extremity function. The RAPAEL smart rehabilitation solution was designed to induce neuroplasticity for hand function of patients with brain damage. The RAPAEL smart glove is a manually functioning recovery device and consists of five bending sensors on the thumb and fingers and a 9-axis inertial measurement unit sensor (three acceleration channels, three angular rate channels, and three magnetic field channels) on the palm of the hand. This solution applied a learning schedule algorithm to game-like exercises so that patients can remain motivated and can find the exercises gradually challenging. The learning schedule algorithm is designed to enhance learning of multiple functional tasks by proposing an optimal challenging task with the proper amount of difficulty. On the basis of the participant’s data such as training progress, prescription, personal interest, and motor function scores, the program computationally selects which game to play and at which level of difficulty. This tool includes several strengths in order to maintain participant’s motivation even in repetitive goal-oriented, task-specific tasks.

2.5 Intervention protocol

The RAPAEL smart glove is designed to customize an exercise by selecting a game and constraining the degree of freedom in the handle to induce targeted movements to more therapeutically desirable movements. The training protocol consists of simple session training modes. The simple training mode involves active range of motion exercises, coordination exercises, cognition (calculation, memory, visual tracking, and visual discrimination) training, timing training, and attention training. The session training mode consists of several patient-selected exercises based on simple training modes to improve specific functions. During the first week of the training period, the participants used only the simple training mode to become familiar with the glove. They initially conducted all the simple training contents such as active range of motion exercises, coordination, cognitive training, timing training and attention training. Subsequently, they conducted participant-selected exercises based on the simple training contents for the following seven weeks. Each week the participants chose a protocol from the non-immersive VR training games with specific exercises. Their therapist instructed the participants on the best ways to maximize the effectiveness of their treatment and their participation in the training program.

The control group played video games as a recreational activity while the intervention group was being treated with non-immersive VR training for the same time periods. In the control group, the video games were chosen by the user and they were commercially available games.

2.6 Outcome measures

Four outcome assessment tools for upper extremity motor function were used. These included the box and block test (BBT); the Jebsen-Taylor hand function test (JTT); the grip strength test; and the Wolf motor function test (WMFT). A clinical assessment tool for non-motor function; the trail making test (TMT), was used in this study (Hung et al., 2019; Mirelman et al., 2016; Triandafilou et al., 2018; Tornbom & Danielsson, 2018; Turolla et al., 2013). The BBT is a clinical tool to examine unilateral gross manual dexterity and is a quick and simple test for measuring upper extremity function. The JTT is a standardized test for assessing overall hand function using seven subtests that simulate the activities of daily living. The JAMAR hand dynamometer (Sammons Preston, Canada) is a standard grip strength data collection tool. The WMFT was designed to assess the upper extremity motor ability of participants. It is useful for differentiating the motor status of chronic stroke patients from a population of higher-functioning individuals with stroke and traumatic brain injuries, in terms of upper extremity motor deficits and their severity. The TMT is a neuropsychological test for assessing visual attention and task switching.

2.7 Statistics analysis

Descriptive statistics, including frequency, mean, and standard deviation, were performed to analyze the common and clinical characteristics of the participants. Differences between bivariate measurements between the two groups were evaluated with a two-way analysis of variance at the conclusion of the non-immersive VR training. The statistical analysis of the data was performed using SPSS version 21.0 (IBM, Co., NY, USA). The level of significance was set at 5%. Statistically significant differences were considered at a two-tailed p-value of < 0.05.

3 Results

Table 1 illustrates the demographics of the 36 study participants who completed the non-immersive VR training or recreational therapy. In the intervention group, there were 14 men and 4 women (mean age, 72.1 years); the time since diagnosis was 14.8 months (6-59 months), height, 165.3 cm (145–182 cm); weight, 70.2 kg (48–92 kg). Of the participants in the intervention group, twelve had infarction, six had hemorrhage, eight had right hemiparesis, and ten had left hemiparesis. In the control group, there were 13 men and 5 women (mean age, 73.2 years); the time since diagnosis was 15.5 months (6–59 months), height, 164.8 cm (145–174 cm); weight, 69.0 kg (48–85 kg). Of the participants in the non-intervention group, twelve had infarction, six had hemorrhage, ten had right hemiparesis, and eight had left hemiparesis. There were no significantly different common characteristics such as age, sex, height and weight between the two groups at the baseline. The clinical characteristics such as time since diagnosis, etiology, paretic side, MMSE score, BBT score, grip strength, JTT, TMT, and WMFT did not differ between the two groups at baseline as shown in Table 1.

In order to investigate the applicability and effectiveness of non-immersive VR training for paretic upper limb recovery, the five clinical parameters were compared and analyzed before and after the intervention. The within-group analysis indicated significant differences in the five clinical outcomes (BBT, JTT, grip strength test, WMFT scores, and TMT time) from baseline after the training in the intervention group (BBT scores, from 27.3 to 34.2; JTT scores, from 56.2 to 68.2; grip strength test, from 19.2 kg to 23.8 kg; WMFT scores, from 73.0 to 81.6; and TMT time, from 42.9 seconds to 35.3 seconds). However, the within-group analysis indicated significant differences in two clinical outcomes (JTT and WMFT scores) in the control group (BBT scores, from 27.1 to 28.8; JTT scores, from 55.6 to 58.4; grip strength test, from 18.4 kg to 18.3 kg; WMFT scores, from 70.4 to 73.2; and TMT time, from 43.0 seconds to 40.1 seconds) as shown in Table 2.

Table 2
Efficacy measures by clinical outcomes for the participants (N = 36)

Variables Intervention group (n = 18) Control group (n = 18) Between-group analysis p-values

Week 0 Week 8 Within-group analysis p-values Week 0 Week 8 Within-group analysis p-values

Box and block test (score) 27.3±8.9 34.2±7.1 <0.001 27.1±10.5 28.8±12.9 0.126 <0.001

Grip strength test (kg) 19.2±8.2 23.8±8.5 <0.001 18.4±4.2 18.3±4.9 0.679 0.001

JTT (score) 56.2±28.7 68.2±31.9 0.001 55.6±26.7 58.4±27.9 0.001 0.475

Trail-making test (sec) 42.9±16.6 35.3±14.3 <0.001 43.0±13.9 40.1±15.3 0.052 0.813

WMFT (score) 73.0±12.9 81.6±7.5 0.002 70.4±12.1 73.2±13.1 0.023 0.032

Variables	Intervention group (n = 18)	Control group (n = 18)	Between-group analysis p-values
Box and block test (score)	27.3±8.9	34.2±7.1	<0.001	27.1±10.5	28.8±12.9	0.126	<0.001
Grip strength test (kg)	19.2±8.2	23.8±8.5	<0.001	18.4±4.2	18.3±4.9	0.679	0.001
JTT (score)	56.2±28.7	68.2±31.9	0.001	55.6±26.7	58.4±27.9	0.001	0.475
Trail-making test (sec)	42.9±16.6	35.3±14.3	<0.001	43.0±13.9	40.1±15.3	0.052	0.813
WMFT (score)	73.0±12.9	81.6±7.5	0.002	70.4±12.1	73.2±13.1	0.023	0.032

JTT, Jebsen-Taylor hand function test; WMFT, Wolf motor function test.

The between-group analysis revealed significant changes in the five clinical outcomes. The results suggest that the intervention group achieved a significantly higher BBT, grip strength test, and WMFT score after training, whereas their scores at baseline were not significantly different from the control group (Table 2). The intervention group showed no significantly higher JTT score or TMT time than that of the control group after 8-weeks of training.

4 Discussion

This study was a randomized controlled trial designed to investigate the effectiveness of non-immersive VR training using the RAPAEL smart glove for improving upper extremity function and cognitive functions compared to that of recreational activities for chronic stroke patients. In this study, we found significant differences in hand grip strength, manual dexterity and arm motor function only in two clinical outcomes at the end of 8-weeks of intervention.

Fig. 1

Flowchart of the enrolment of participants in the study trial based on the selection criteria.

In general, stroke survivors may be discharged after their postural control and gait performance are restored to levels that would enable independent daily living. It is essential to continue the training in order to increase upper extremity function in an outpatient rehabilitation setting. In this regard, the accessibility of the rehabilitation center and adaptability of the therapeutic program are important for continuous participation in the treatment program after discharge. This study used non-immersive VR training due to its’ several beneficial points such as lower cost, lower complexity, and easier adaptability than immersive VR training (Saposnik et al., 2016). In a patient group with long-term permanent disability, the continuous expenditure to undergo a rehabilitation program is burdensome. In addition, easy access to a rehabilitation program is important for those who need to participate continuously in rehabilitation treatment. The severity of the disability in reaching, grasping and manipulation of objects determines the level of independence in daily living and community-dwelling after a stroke. We used the RAPAEL smart glove system which is a low-cost commercial gaming system as an alternative way of delivering non-immersive VR training. The RAPAEL smart glove consists of a smart glove, with a 9-axis movement and position sensor, and a rehabilitation program that requires various physical motions such as activities of daily living-related tasks. The program provides both entertainment and clinical effectiveness. The participants performed various functional activities with the RAPAEL smart glove, such as cooking and fishing in a VR environment as well as functional activities to maintain their motivation and interest in the rehabilitation environments.

Park et al. assessed the effectiveness of using the RAPAEL smart board as an assistive tool for therapists in clinical rehabilitation therapy settings for improving the motor recovery rate of stroke survivors (Park et al., 2018). They reported using the RAPAEL smart board in combination with traditional treatment and achieved a significantly improved motor recovery compared to traditional treatment alone in stroke survivors (Park et al., 2018). In addition, Jung et al. examined the feasibility of using the RAPAEL smart glove as an assistive tool for therapists in clinical rehabilitation therapy settings (Jung et al., 2017). They also reported the wearable sensors and therapeutic games improved the motor recovery rate of stroke survivors (Jung et al., 2017). The results of this study show the improvement of upper extremity physical function and cognitive speed.

To improve the upper extremity function for reaching, grasping and manipulating objects, previous studies used non-immersive VR training with commercial game platforms (Askin et al., 2018; Esfahlani et al., 2018; Hung et al., 2019; Mouawad et al., 2011). They suggest that non-immersive VR technologies improve upper extremity function. However, Saposnik et al. reported that the effectiveness of non-immersive VR technologies added on to conventional therapies for subacute stroke patients was not significant compared to recreational activities, which are simple, low cost, and widely available games (Saposnik et al., 2016). The participants in this study also received non-immersive VR training, similar to the subjects of the study by Saposnik et al., however the intervention group showed significantly greater improvement in upper extremity function in terms of the BBT, JTT, grip strength test, and WMFT scores, after non-immersive VR training than the group that performed recreational activities for chronic hemiparetic stroke.

Several studies have reported the effectiveness of cognitive training applied with games-based VR training for stroke survivors (Cameirao et al., 2016; Faria et al., 2016; Gamito et al., 2017). In one of their studies, Faria, et al., reported that VR tools showed potential for improving cognitive rehabilitation through a VR-based intervention for stroke survivors. The results of that study showed significant improvements in global cognitive functioning, attention, memory, visuo-spatial abilities, executive functions, and emotion after VR training. They also used TMT as a clinical tool to improve attention and executive function after VR training for stroke patients (Faria et al., 2016). In another study, Gamito et al. reported the effectiveness of a VR application in neuropsychological rehabilitation for improving attention and memory function in stroke survivors (Gamito et al., 2017). To evaluate the effectiveness of non-immersive VR training for improving cognitive function, this study also measured the TMT before and after the intervention in the participants. However, the non-immersive VR training in the intervention group did not differ from TMT times compared to the recreational activities used by the control group. Based on the results of this study, cognitive function in the chronic phase following a stroke would require more continuous training. This study conducted training with chronic hemiparetic stroke patients in 24 sessions for 8 weeks.

This study evaluated the effects of non-immersive VR training using a RAPAEL smart glove on the upper extremity and cognitive functions of chronic stroke survivors. The results of this study showed the beneficial effects of non-immersive VR training for improving upper extremity function in chronic stroke patients. The study performed a blinded assessment to control the causal validity, however conventional therapeutic effects, history, test effects and regression effects could not be controlled. Therefore, future studies with a double-blinded, multi-center research design and randomized controlled trials for hemiparetic stroke survivors in any recovery period are required. This study did not investigate the follow-up period after 8 weeks of training. Future research will examine the follow-up and retention of the therapeutic effects of non-immersive VR training for chronic hemiparetic stroke.

Conflict of interest

The authors have no conflict of interest, whether personal, academic, or financial, that may bias their decisions or actions in relation to the publication of this article.

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