Virtual Reality Therapy for Patients with Stroke · Virtual Reality With a greater understanding of the nature of brain plasticity, stroke rehabilitation continues to gravitate toward

Virtual Reality Therapy for Patients with Stroke

Volume 1 • Issue 2 • 1000105Aging SciISSN:JASC an open access journal

Open AccessReview Article

Journal of Aging ScienceLeBlanc et al., Aging Sci 2013, 1:2

http://dx.doi.org/10.4172/jasc.1000105

Keywords: Virtual reality; Chronic stroke; Aging; Rehabilitation; Neuroplasticity

Abbreviations: BBT: Box and Block Test; JTHF: Jebsen Test of Hand Function; PMP: Proximal-metacarpal-phalanx; RCT: Randomized Controlled Trial; ROM: Range of Motion; SAILS: Structured Assessment of Independent Living Skills; UE: Upper Extremity; VE: Virtual Environment; VR: Virtual Reality; ADL: Activities of Daily Living; SORT: Strength of Recommendation Taxonomy; ICF: International Classification of Functioning

IntroductionWorldwide, stroke remains the leading cause of long-term motor

disability among adults [1-4]. As the population continues to age, so too, will the risk of stroke, with more than two-thirds of strokes affecting those over the age of 65 [5,6]. One of the many positive achievements of modern medicine has been the decrease in mortality rates following stroke. As such, the number of older individuals surviving stroke and in need of motor rehabilitation is predicted to see inevitable increases due to the long-term sequelae associated with stroke [2,6,7]. The majority of survivors of stroke will experience UE deficits, and for approximately 55-75% of these individuals, the deficits will endure well beyond the time of injury [8]. As such longstanding impairments hold the power to substantially reduce one’s quality of living [9], the degree of motor and functional recovery attained is often a pivotal influence in whether a stroke is deemed debilitating [10].

A Plastic BrainFollowing a stroke it is essential for the brain to undergo

reorganization in order for motor recovery to occur [7]. For decades, neuroscientists suggested that the mature central nervous system was static in nature, encompassing little capacity to restructure, and by that means, repair itself [11,12]. However, it has since been established that not only is the human brain capable of such plastic changes, it is always changing [11,12]. This ongoing neural activity is appropriately termed

*Corresponding author: Stephanie LeBlanc, School of Rehabilitation Sciences, McMaster University, Canada, E-mail: [email protected]

Received March 14, 2013; Accepted March 16, 2013; Published June 18, 2013

Citation: LeBlanc S, Paquin K, Carr K, Horton S (2013) Non-immersive Virtual Reality for Fine Motor Rehabilitation of Functional Activities in Individuals with Chronic Stroke: A Review. Aging Sci 1: 105. doi:10.4172/jasc.1000105

Copyright: © 2013 LeBlanc S, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Non-immersive Virtual Reality for Fine Motor Rehabilitation of Functional Activities in Individuals with Chronic Stroke: A ReviewStephanie LeBlanc1*, Kate Paquin2, Kelly Carr2 and Sean Horton2 1School of Rehabilitation Sciences, McMaster University, Hamilton, ON, Canada2Department of Kinesiology, University of Windsor, Windsor, ON, Canada

AbstractMore than two thirds of the individuals who have strokes are over the age of 65. Therefore, as the global

population continues to age, the risk of stroke is expected to increase substantially. Virtual reality (VR) is an emerging therapy that holds promise for the rehabilitation of patients with chronic stroke conditions. VR is an interactive, computer-based simulation of real life tasks, occurring in real time. The aim of this review was to explore whether non-immersive VR could be used to effectively improve fine motor function of the affected upper extremity in patients with chronic stroke. Ten studies examining non-immersive VR for the purpose of chronic stroke rehabilitation were included for review. Studies utilized a variety of VR-based interventions, reporting trends toward improvement on nearly all outcome measures. Results were examined at the levels of “body structure and function” and “activity” according to the International Classification of Functioning. Across the studies, significant improvements were reported for the Jebsen Test of Hand Function, the Box and Block Test, participants’ finger fractionation, finger tracking measures, and time from peak hand velocity to movement of an object. However, considerable variability in participants’ recovery rates of fine motor function across the studies suggests that the results should be interpreted with caution. More research using randomized controlled trial designs will clarify evidence surrounding the amount of improvement that can be experienced with non-immersive VR-based interventions. This review provides justification for continued investigation within the field of motor skill recovery in patients with chronic stroke.

neuroplasticity, which can be described as the brain’s natural tendency to reorganize itself in response to changing internal and external demands [1,13]. Stroke rehabilitation has become a popular platform for neuroplasticity-related research, as motor recovery from stroke aptly demonstrates the brain’s malleability and capacity for ‘rewiring’ post-injury [11]. It is of importance to note that this plasticity exists as a function in both healthy and damaged brains alike [14]. Furthermore, the brain’s remarkable ability to promote repair following a stroke has been observed to extend years beyond the initial injury [4,15].

The Motor Recovery ‘Plateau’ Despite this notion of an incessantly plastic brain, the majority of

recovery of general motor function has typically been observed within the first six to twelve months post-stroke [12,16]. The rate at which recovery occurs appears to decelerate as time passes, with recovery most rapid in the first month, slowing in subsequent months, and eventually reaching a ‘plateau’ [15,16]; that is, a point in time during the course of rehabilitation in which a patient no longer exhibits signs of improvement in response to therapeutic intervention [15]. This observable plateau holds serious implications for stroke survivors, as this perceived cessation of progress often provides the grounds for discharge from rehabilitative programs [17,18]. As such, reservations regarding the cost-effectiveness are warranted, since the apparent widespread presence of a motor recovery plateau suggests a limit to


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late functional recovery of survivors of stroke [19,20]. Accordingly, as stroke recovery nears the more stable, chronic stages (greater than twelve months post-stroke), doubt pertaining to the effectiveness of a motor-rehabilitation intervention rises, and patients are often denied any further treatment [19-21]. Nevertheless, this proposed motor recovery plateau has not gone without opposition. Rather than explain stroke-related plateaus as a diminished capacity to manifest any further motor gains, Page, Gater and Bach-y-Rita (2004) have likened the plateau to the neuromuscular adaptation that occurs after exercise in healthy adults. Despite operating on similar principles, the common response to such adaptations differs greatly. When a healthy adult experiences neuromuscular adaptation to exercise, the routine is subsequently varied or intensified to facilitate positive change; not terminated [18]. It has been argued that individuals with strokes experience neuromuscular adaptations to rehabilitative exercise, however, in contrast to their healthy counterparts this adjustment to treatment commonly results in the discontinuation of therapy [18]. In addition to disagreements surrounding the nature of the plateau, some question its susceptibility to external influences [17,18]. Demain et al. [17] suggest that the plateau is inherently complex, and expose the ambiguity surrounding its current conceptualizations. There is reason to believe that patient-related factors, therapist values, services provided, and the dynamic patient-therapist relationship all play a part in a patient’s respective recovery [17]. Both Page et al. [17] and Demain et al. [18] note that a therapist’s acceptance of such a plateau may in fact limit patients’ expectations for recovery, thereby inhibiting success by way of a self-fulfilled prophecy. Though the mechanics underlying the plateau are not entirely understood, promise that the motor recovery plateau can be overcome is held, to some extent, in the emergence of successful cases of chronic-stroke recovery [15,20,22-31].

Rehabilitation for ‘Chronic’ Stroke The window of time for the effective application of restorative

therapies is not entirely clear, and remains highly variable between patients [15]. Although early rehabilitation has been deemed more effective, motor recovery in the chronic stages of stroke has been observed, and can be attributed, in part, to physical rehabilitation [15,17,22-31]. A meta-analysis conducted by Ferrarello et al. [20] concluded that in comparison to no treatment or a placebo, motor rehabilitation applied to patients with chronic strokes improved both motor and functional outcomes of recovery. Still, due to the scarcity of high-quality, conclusive evidence of the effectiveness of late rehabilitation, it is uncommon for patients having chronic stroke to be offered physical therapies [20,32]. Evidently, further research surrounding the cost-effectiveness, practicality, and best practice of late rehabilitation is required before any definitive change can be made [9,20].

Virtual Reality With a greater understanding of the nature of brain plasticity, stroke

rehabilitation continues to gravitate toward therapeutic approaches that capitalize on these insights, in an effort to address the limitations of conventional rehabilitation practices, and to optimize functional outcomes [33,34]. Among these approaches is VR, a computer-based technology that allows users to interact with a simulated environment and receive continuous, immediate feedback related to performance [34-36]. Since motor recovery following stroke has been found to be experience-dependent, it is vital to employ rehabilitative interventions that facilitate quality experiences, which serve to bolster neuroplastic change [9,33]. Kleim and Jones [33] highlighted several

principles related to experience-dependent neuroplasticity that can be incorporated into rehabilitation of the damaged brain, including intensity, repetition, specificity, and salience. Intensity refers to the number of hours of consecutive therapy that a patient receives, whereas repetition refers to the number of times a particular learned behavior is practiced [33]. Table 1 (Included as supplementary data) outlines the studies’ protocols as well as the total number of hours of therapy received by each participant. Specificity is used in reference to the training of specific purposeful and skilled tasks, with the intent of learning or re-learning that task [33]. Last, salience relates to a patient’s engagement in therapy, achieved through sufficient motivation and attention, which adds greater level of importance to the task [33]. VR lends itself well to the application of such principles, given its capacity to encompass task-specific training, appropriate intensities and repetition, and salient experiences [33,35-39]. Furthermore, VR systems can be tailored to the individual needs of a patient, to include meaningful, challenging, and progressive exercises that can be carried out in a variety of settings. This flexibility supports high-intensity, repetitious training that patients find motivating, engaging, and enjoyable [22,30,33,40]. VR-based therapy can be classified on a continuum from fully immersive to non-immersive, dependent on the degree to which the user is perceivably immersed in the VE [34,41]. Immersive VR allows the user to feel that they are situated within the VE presented to them; a concept termed “presence” [36]. This presence can be achieved and reinforced through the use of a variety of equipment both worn by, and in front of the user (e.g., cave systems, large screen projections, head mounted displays, and specially designed stereoscopic glasses) [27,36]. In contrast, non-immersive VR can be likened to looking through a window at a scene, and often involves the use of smaller-scale, 2-dimensional screens (e.g., computer or television screens), with or without the use of interface devices (e.g., Cyber glove, joy stick, or computer mouse) [27,36,41,42]. Also considered non-immersive VR are commercially available computer and video gaming systems [34]. These systems have been adopted by clinicians as accessible and relatively low-cost alternatives to expensive therapeutic technologies, though not specifically designed for rehabilitative purposes [34].

The Benefits and Challenges of Virtual Rehabilitation Promising evidence exists for the use of non-immersive VR as a

supplement to conventional rehabilitation practices for persons with stroke [41,43-46]. As with any modality for stroke rehabilitation, the implementation of VR is accompanied by both benefits and challenges (Table 2). This is by no means an exhaustive, nor an indisputable listing; however the abundance of perceived benefits warrants further exploration of VR for therapeutic purposes. The identified challenges are justified given the relative novelty of virtual rehabilitation, and may partially be founded in unfamiliarity, among both therapists and clients, regarding both the technology and its potential value within therapeutic settings. As such, some of these challenges will perhaps be resolved through continued exposure and enhanced awareness [47-50]. Nonetheless, the numerous challenges will need to be addressed through additional research in order for a widespread acceptance of VR for rehabilitation to materialize.

Purpose of ReviewAssociated with our aging population is an increasing demand for

stroke-related motor rehabilitation [5,6]. As UE deficits have been found to endure for years beyond injury in some patients, the need for effective late-rehabilitation practices is of vital importance [8]. Stroke-induced hemiparesis affects fine motor control, which can dramatically impair



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Benefits ChallengesProvision of a non-threatening practice environment, which may prove dangerous otherwise (e.g., preparing a hot beverage or operating a motor vehicle) [47]

Therapists’ resistance to technology (e.g., for fear of being replaced, or lack of conviction in its effectiveness) [40,47]

Simulation of objects and events that closely resemble those in real-world settings [43] Lack of clinical acceptance due to the paucity of evidence surrounding factors such as cost effectiveness or feasibility [40,47]

Flexibility that allows for highly individualized learning environments [48]Many virtual interfaces have not been designed for medical purposes, raising issues of patient safety (e.g., adequate sterilization for repeated use may be problematic) [36,40]

Ability to accommodate for a wide spectrum of cognitive and physical impairments [29,40,47]

Commercial equipment that is unable to adequately accommodate all physical impairments [36,40]

Low cost associated with commercially available VR systems [47,49] Unaffordability of VR software and associated hardware for individuals and organizations that lack subsidy [36,40]

Potential to increase patient enjoyment, motivation, and thereby adherence [29,40,47,49] Patients’ negative perception of VR [36]

The potential for telerehabilitation in a variety of patient environments, absent of direct therapist supervision [40,49,50] Lack of patient compliance in the absence of direct therapist interaction [40]

Adjustable task-related variables according to patient’s abilities (e.g., increasing the speed of tasks based on a patient’s progress) [29]

Digital measurement and tracking of patients’ progress [47] Constraints to encourage error-free learning (e.g., a virtual piano only emitting sound when the correct key has been pressed) [47]

Increased independent practice time, and task repetition [29,40,47,49] Same VR hardware can be used for various different exercises, as well as for various different patients [40,47]

Offers real-time visual and potentially force feedback to user [29,47]

Table 2: Overview of the perceived benefits and challenges of non-immersive VR for stroke rehabilitation extracted from the literature.

a person’s ability to live independently, perform ADL and participate in leisure activities and productive work [51,52]. Non-immersive VR is a rehabilitative approach that has gained support in recent years, and shows promise for its ability to promote motor restoration through the application of neuroplastic principles [36]. Therefore, the purpose of this review is to explore the effectiveness and user perspectives of non-immersive VR for the rehabilitation of fine motor skills of the UE in patients with chronic stroke.

MethodsIdentification of relevant studies

The literature was reviewed by three researchers to identify published studies including RCT case studies, and pre-test/post-test study designs that focused on the use of non-immersive VR in fine motor UE rehabilitation of patients with chronic stroke (more than 12 months post-stroke). The following databases were searched: OVID-MEDLINE, EMBASE, Scopus, CINAHL, Pro Quest Science and Technology, and Google Scholar. These databases were searched using the following key terms:“virtual reality”, “virtual environment”, “commercial gaming”, and “non-immersive” in combination with “stroke”, “rehabilitation”, “treatment”, “fine motor” and “chronic” or “late-stroke”. Additionally, the reference lists of each retrieved article were reviewed in order to identify other pertinent articles.

Eligibility criteria

Inclusion criteria were (1) English-language articles that examined the effectiveness of (2) non-immersive VR for (3) fine motor rehabilitation of the UE in (4) individuals having chronic stroke, and (5) studies incorporating a combination of both VR-based and conventional exercises (i.e., augmented VR). Exclusion criteria were (1) conference proceedings and abstracts, (2) studies on individuals with acute or subacute stroke conditions at the onset of the study (less than 12 months post-stroke), (3) studies utilizing specially designed assistive technology, (4) studies focusing on gross motor rehabilitation (e.g., gait or balance-related activities), (5) studies using fully immersive

(VR) technology (e.g., large screen projections, cave systems, head-mounted displays, force-plate technology, and assistive robotics). Last, (6) wrist measurements alone did not suffice as grounds for inclusion when involved in gross motor movements, such as reaching (e.g., wrist displacement), as fine motor will refer only to those manual movements predominantly produced by the smaller muscles or muscle groups of the UEs.

Quality appraisal

The methodological quality of the included studies was assessed according to the SORT [53]. Studies were not excluded on the basis of the SORT evaluation; rather, this information was used to substantiate recommendations according to the quality, quantity and consistency of the reviewed studies. According to the SORT, the quality of individual studies was rated 1, 2, or 3, while the strength of a recommendation based on the overall body of evidence was graded as A, B, or C [53]. A level-1 indicated good quality, patient-oriented evidence, a level-2 indicated. limited-quality, patient-oriented evidence, and a level-3 indicated non–patient-oriented evidence or other evidence [53]. In terms of the strength of recommendation, a grade-A indicated a recommendation based on consistent and good-quality, patient-oriented evidence, a grade-B indicated a recommendation based on inconsistent or limited-quality patient-oriented evidence, and a grade-C indicated a recommendation based on consensus, usual practice, opinion, disease-oriented evidence, or case series for studies of diagnosis, treatment, prevention, or screening [53]. According to these criteria, the selected studies were rated as level-1 (n=1), level-2 (n=4), and level-3 (n=5), with an overall recommendation strength grade-B (recommendation based on limited-quality patient-oriented evidence). Please refer to Table 1 (Included as supplementary data) for specific SORT levels.

Sample study characteristicsNine research articles provided the ten selected studies under

review ([26] published two research studies within a single article). The majority of the ten selected studies were case studies (n=5), followed by



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studies using a pre-test/post-test design (n=4), and one study employed a RCT design. Most studies had participants engage solely in VR-based rehabilitation strategies (n=8) with three studies augmenting VR rehabilitation strategies with traditional exercises to improve fine motor skills. With respect to all of the articles reviewed, the participants’ (n=60) ages ranged from 42 to 85 years, with participants between 1 and 8 years post-stroke ( Table 1 (Included as supplementary data)).

Outcome measuresWithin the ten selected studies, a variety of methods were used

to measure fine motor skills of the affected hand post-stroke (Table 1 (Included as supplementary data)). At the “body structure and function” level of the ICF [54], outcome measures were finger and hand movement parameters, including measures of finger and thumb speed and strength, finger and thumb ROM, finger fractionation, peak hand velocity, kinematic analysis of prehension movements, and finger tracking accuracy. Similarly, at the “activity” level of the ICF [54], outcomes included the JTHF; (n=8), the BBT (n=1), and the SAILS (n=1). Eight studies involved measurement at both “body structure and function” and “activity” levels to assess fine motor ability, while the remaining two studies used only measures of “body structure and function” or “activity” [54]. The JTHF was developed as a short, objective evaluation of basic hand functions relative to ADL, and consists of seven subsets that provide a broad sampling of functional tasks [55]. The test items include a range of fine motor, weighted and non-weighted manual activities, including writing, turning index cards, picking up small common objects, simulated feeding, stacking checkers, picking up large light objects, and picking up large heavy objects [55]. The BBT is a quick and simple measure of unilateral gross manual dexterity [56]. It requires participants to grasp and move as many blocks within 60 seconds from one side of a divided box with the tip of the index finger and tip of the thumb of the paretic hand and release the block on the opposite side of the box [24]. The SAILS is an assessment of functional abilities associated with ADL [57]. It directly assesses 10 areas of everyday functioning: fine motor skills, gross motor skills, dressing, eating, expressive language, receptive language, time and orientation, money-related skills, instrumental activities, and social interaction [57].

ResultsThe results from ten research studies examining VR-based

rehabilitation for fine motor skills during the chronic phase of stroke have been reviewed. According to a SORT assessment the quality of the individual studies ranged from level-1 through level-3, with an overall strength of recommendation of grade-B. The study type, SORT level, specific exercises performed, intervention protocol, total hours of VR exercise, and the outcome measures for each study are included in Table 1 (Included as supplementary data). To avoid redundancy, we have identified all outcome measures that were used on one occasion. Please refer to Table 1 (Included as supplementary data) for specific results. Outcome measures utilized in two or more studies are compared and summarized below.

Body structure and function level

Finger and thumb ROM: Results of seven studies unanimously indicated a trend toward improvement in finger and thumb ROM following VR-based rehabilitation [22,24,26,28-30]. While improvements were found in each of these studies, only two reported findings that reached a level of statistical significance [24,30]. Carey et al. [24] reported that finger and thumb ROM significantly increased in participants provided with a pathway to follow on the virtual

interface (track group), while participants without this pathway (move group), experienced no change. As only the track group was trained to increase their ROM using tracking protocols with amplitudes at 125% of their range, these findings were expected. Merians et al. [30] also reported a significant improvement from pre-therapy to post-therapy, with performance after a one-week retention period remaining significantly better than pre-therapy performance. It is worth noting that individually reported data contained in four of the seven articles measuring finger and thumb ROM revealed a wide range of change in thumb (-40% to 148%) and finger ROM (-9 to 27%) suggesting little consensus regarding expected improvement in finger and thumb ROM through VR rehabilitation late-stroke [26,28,30].

Finger and thumb speed: Six studies assessed finger and thumb speed [22,26,28-30]. While five of these reported improvements following VR rehabilitation, only one study reported findings at a level of statistical significance, as measured by a CyberGlove [30]. Furthermore, when assessed following a one-week retention period it was found that finger and thumb speed were significantly better than pre-therapy levels [30]. Despite overall positive outcomes, individualized rates of recovery (presented as a percentage) demonstrated considerable variability, with thumb speed change ranging from -7% to 80%, and finger speed change from -1% to 78% [26,28,29].

Finger fractionation: Six studies reported improvements in finger fractionation (i.e., the assessment of participants’ isolated finger control) following VR therapy [22,26,28-30], however only two of these studies reported significant improvements [22,30]. Merians et al. [30] reported that these improvements were maintained above pre-therapy levels after one week without participating in VR rehabilitation. Similar to the above impairment measures, there was considerable variability regarding the improvement in finger fractionation of chronic stroke patients, with changes ranging from -22% to 118%, with an average increase of 50% [22,26,28,29].

Ability of fingers and thumb to do mechanical work: Mechanical work was estimated as the force exerted by the thumb or fingers in relation to their displacement [30]. One of five studies examined the statistical significance of changes in mechanical work done by the fingers and thumb, and reported that there was no significant increase in this measure of fine motor skills [30]. However, through the use of percentage measures, the remaining four studies suggested a 29% average increase in the ability of the fingers and thumb to do mechanical work. This increase should be interpreted with caution as the results varied greatly, with changes ranging from -18% to 102% [26,28,29].

Peak hand velocity: Two studies examined the time elapsed from peak hand velocity to the moment an object is lifted off a table [22,30]. Adamovich et al. [22] reported no change in time to peak velocity following VR therapy, however, this finding was to be expected as participants’ elbow and shoulder were not trained during therapy. In contrast, time from peak velocity to the moment the object was lifted from the table did decrease significantly; performed 22% faster on average following intervention [22]. This finding suggested an increase in the participants’ ability to appropriately match their finger positions to the shape of the object [22,30]. Similarly, Merians et al. [30] found that despite a lack of change in peak hand velocity, participants’ time from peak velocity to the moment the object was lifted from the table significantly decreased. On average, participants performed this task 19% faster after the intervention, again illustrating a transfer of improvement to a real-world task [30].



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Activity level

Jebsen Test of Hand Function: Eight studies used the JTHF as an outcome measure, primarily to assess the transferability of improvements to functional tasks [22,24-26,28-30]. Overall, the studies suggest that VR rehabilitation during the chronic phase of stroke can significantly improve performance on the JTHF [22,24,26,30]. Though the remaining studies that used the JTHF as a measure of fine motor skills did not provide significance values, each provided results indicative of improvement following VR therapy [25,26,28,29].

DiscussionStroke is the leading cause of long-term disability among adults [1-

4]. In order for motor recovery to occur following an injury such as a stroke, neural reorganization is imperative [7]. Neuroplasticity, a term used to describe this reorganization of the brain, has sparked substantial research surrounding motor recovery post-stroke [1,13]. However, there is a limited number of quality studies focused specifically on the use of VR interventions for fine motor rehabilitation in chronic stroke patients. Since VR is a novel rehabilitative approach within this population, it is important to review the preliminary evidence to allow for meaningful and timely progression. Therefore, the purpose of this review was to examine the effectiveness of non-immersive VR-focused rehabilitation for improving UE fine motor skills in chronic stroke patients. As a whole, the articles reviewed suggest that VR rehabilitation may yield positive changes in individuals’ motor recovery in the years following their stroke. Within the ten studies, a variety of methods were used to measure fine motor skills of the affected UE post-stroke, at both the “body structure and function” and “activity” levels of the ICF [54]. At the level of “body structure and function,” several measures indicated improvements, with the exception of measures of finger strength and finger extension [22-26,28-30,58]. Among these measures, significant improvements were found in participants’ finger fractionation [22,30], finger tracking [24], and time from peak hand velocity to the moment an object was lifted from a table [22,30]. However, these results should be interpreted with caution given the considerable variability between participants’ degree of change. At the level of “activity” [54], the JTHF, BBT, and SAILS were used as measures. These measures were primarily used to determine transferability of gains from VR therapy to real-world tasks. The JTHF was utilized by eight of the reviewed studies; of which five reported significant improvements [22,24,26,30]. Furthermore, significant improvement in participants’ performance on the BBT was reported, however no change was reported in the participants’ SAILS scores following VR intervention [24,40]. Included within this review, only a single study utilized either of these measures (i.e., the BBT or SAILS), making comparison between studies impossible. Further research utilizing these particular outcome measures is required in order for the development of any definitive conclusions.

Experience-induced neuroplasticity

It is feasible that the positive findings throughout the reviewed studies were at least partially a result of the facilitation of cortical reorganization by VR intervention. Each of the studies demonstrated the application of various neuroplasticity-bolstering principles, including task-specific training, high intensity and repetition, salience, and novelty [33]. As previously mentioned, the intensity of each intervention was operationalized as the total number of hours of consecutive therapy a participant received. Intensities (Table 1 (Included as supplementary data)), ranged from a minimum of 15 minutes to a maximum of 5 hours of total therapy per day. When considered with the duration of each study, the total number of hours of therapy received

by each participant ranged from 2.5 hours to 45 hours. Despite similar findings among studies, there remains a lack of definitive conclusions about appropriate intensities due to the variability of these components in the study protocols. For example, significant improvements on the JTHF were reported by studies with a wide range of intensities and durations [22,24,26,30]. This would suggest that mechanisms beyond intervention intensity were responsible for these gains in function, or that just 15 minutes of intensive therapy each day might be sufficient in producing such gains. However, it is of importance to note that despite its short duration and intensity (minimum 2.5 hours, and minimum 15 minutes per day, respectively) this intervention employed a high degree of repetition [24]. That is, each participant was required to perform 180 trials (each lasting between 5 and 15 seconds) each day, for 10 days [24]. Therefore, this high degree of task-specific repetition may have been sufficient for facilitating neuroplastic changes.

Another important mechanism of neuroplasticity, perhaps compensating for lower intensities and short durations, was likely the salience facilitated by each of the VR interventions [33]. Though not explicitly stated consistently, the novelty and ‘play’ component associated with each of the VR interventions is believed to have fostered greater participant enjoyment, motivation, and thereby engagement as compared to conventional rehabilitation practices [20,30,33]. It is possible that participants’ attention was heightened and that skills were performed with greater purpose and effort. Therefore, the novelty, interactive nature, and game-like characteristics may have fulfilled the requirements of salience needed for the learning of tasks, resulting in greater neuroplastic change and overall functional gain [33]. Within the studies reviewed, the notion of VR-augmented therapy was explored [26,28,29]. The conventional exercises encompassed functional fine motor tasks, including: the placement of paper clips [26,28,29], moving checkers [28,29], and arranging pegs on a pegboard [28,29]. Interestingly, all three augmented VR studies noted an increase in thumb ROM, whereas only one of the standalone VR studies did [26]. Beyond increased thumb ROM, the augmented VR studies yielded similar results to the standalone VR studies (e.g., improved finger fractionation, finger speed, and JTHF scores) [22,24,26,28]. This offers practical implications for therapists and researchers without the means necessary to run a conventional rehabilitation program, or for those looking to augment an existing program with VR. Researchers questioned whether the changes found in participants’ performance were due to VR training, conventional training (i.e., non-VR training) that augmented the VR training, or a combination of the two [28]. Merians et al. [30] opted for the elimination of non-VR tasks from the study thereby crediting any changes in functioning to VR-based interventions. In support of this objective, Merians et al. [30] found that training in an environment that was entirely VR-based elicited motor recovery changes that did in fact translate to real world functional tasks, as demonstrated by changes on the JTHF. Further research comparing outcome differences between augmented and standalone VR in chronic stroke is needed.

Benefits and challenges

Key benefits noted throughout the literature reviewed were participants’ enjoyment, motivation, engagement in, and acceptance of VR therapies [23,26,28,29,41]. Researchers explored the positive influences of VR interventions through the monitoring of participants’ attendance, mood, engagement, and willfulness to adapt to the VR training [23,26,28,29]. Interestingly, participants who initially expressed a negative attitude toward VR training developed a more positive attitude or ‘spirit’ over time [23]. Such positive attitudes



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were exemplified through maintained attendance, including punctual attendance and willingness to make up for missed appointments, throughout the intervention [23]. Following one VR intervention, participants reported feeling that continued participation in VR would lead to further gains, and wished that they had participated in VR therapy sooner [28]. Similarly, Lewis et al. [59] found that despite a lack of clinically significant gains, perceived gains were made in participants’ hand function, and participants reported increased ease in terms oftheir performance of ADL.

User perspectives

The sustainment of VR-based interventions in physical rehabilitation is heavily influenced by the perspectives of its users [59]. Lewis and colleagues examined user perspectives toward a VR intervention in order to better understand which of its aspects were considered most important. Several themes emerged across user responses, including: (1) stretching oneself, (2) purpose and expectations, and (3) future improvements. Stretching oneself related to performing a novel activity and challenging oneself physically, mentally and socially [59]. In challenging participants’ current ability, participants reported stretching themselves into areas that they had not previously explored. Responses pertaining to purpose and expectations of VR revealed that the users only wished to use VR in the context of rehabilitation, as opposed to using it for entertainment purposes [59]. Expectations of VR were influenced by previous experiences in rehabilitation, with users reporting that augmented VR in rehabilitation was most favorable. The users also offered ideas for future improvement surrounding the VR intervention [59]. The most common suggestions included: improvements to the scoring systems to include increased provision of performance feedback, decreasing distractions, enhancing the realism and accuracy of the VE, and the incorporation of a competitive component [59]. Ultimately, acceptance of a VR intervention relies on participants’ ability to achieve control, experience success, and maintain an environment in which they are constantly challenged and thereby progressing [59]. A VR intervention that facilitates the experience of these factors holds the ability to promote enjoyment, motivation, and heightened commitment to the rehabilitation process as a whole [41,59].

Commercial gaming as a cost-effective alternative The costs associated with VR systems can make their use in

rehabilitation settings impractical for patients and therapists alike [30]. A more affordable alternative to clinically designed VR is commercial gaming systems. To date, academic literature focused on the use of commercial gaming for chronic stroke rehabilitation is lacking. Furthermore, the paucity of research studies examining commercial gaming for fine motor rehabilitation in individuals with chronic stroke meant that an accurate portrayal of its effectiveness could not be ascertained. Due to its prospects as an inexpensive modality for VR therapy however, findings related to commercial gaming for rehabilitation of the UE post-stroke will be briefly explored. Commercial gaming has evolved into a user-friendly and affordable entity, in comparison to its preexisting models [40]. As such, community level rehabilitation settings with limited access to funding may now be able to afford commercially available VR systems [49]. This possibility holds substantial promise for those with chronic stroke, as it is predominantly through community-based rehabilitation programs that stroke patients receive therapy following discharge from inpatient and outpatient services [49]. This potential for application extends beyond community-based rehabilitation and may also be implemented

as a means for home-based therapies [60]. Rehabilitation intervention studies utilizing commercial gaming have provided further support for its effectiveness in eliciting functional gains and trends toward improved quality of life [51,61,62].

Limitations and future directionsThe generalizability of the findings in this review is limited for a

number of reasons. Neither stroke type, nor severity were reported or analyzed, however, both hold several practical implications for the applicability of the findings. Future studies should investigate the impact that the severity and type of stroke has on motor recovery outcomes following VR treatment in the chronic stage of stroke. Intensity and duration of the treatment protocols, as well as outcome measures among the included studies varied considerably, hampering our ability to make robust conclusions about the findings due to this heterogeneity. With respect to the inclusion of studies, only published studies were included which may have resulted in a publication bias toward more positive results. Last, the quality appraisal of the evidence according to the SORT [53], revealed the studies as being primarily level-2 or -3, allowing for grade-B recommendations based on their cumulative findings. The rating of the studies is indicative of limited-quality, patient-oriented evidence and case studies, which hinders our ability to indisputably attribute positive gains to VR-based interventions. The included studies provide a strong foundation for future research conducted in this area; however, evidence-based recommendations for practice contexts based on these findings are necessarily speculative at this time, provided that research surrounding VR for fine motor rehabilitation of individuals with chronic stroke is in its infancy.

ConclusionIt was once believed that the brain was a static and irreparable

entity [11,12], however, there is now growing evidence to support examination of the long-term rehabilitative effects following a stroke, thereby warranting research beyond the gains achieved solely during the acute and sub acute stages of stroke recovery [11,12,15,20,22-26,28-31]. Although not yet widely established in stroke rehabilitation, VR training possesses the qualities to be a valuable rehabilitative tool for motor function in chronic stroke patients. The use of VR as a tool for patients in the late stages of stroke recovery has been explored for over a decade; however the number of studies concerned with fine motor rehabilitation remains limited. As evidence accumulates in support of this notion, patients with chronic stroke who were once believed to be incapable of further rehabilitative gains will have greater opportunity to work toward furthering their motor recovery. It is well known that the recovery of both gross and fine motor movements is important for the completion of ADL, and thereby, an increased quality of life [51,52]. As such, further research into the rehabilitation of fine motor control post-stroke should be conducted in order to determine just how viable and effective VR is as a therapeutic medium among those with chronic stroke.

References1. Rossini PM, Calautti C, Pauri F, Baron JC (2003) Post-stroke plastic

reorganisation in the adult brain. Lancet Neurol 2: 493-502.

2. Sacco RL, Frieden TR, Blakeman DE, Jauch EC, Mohl S (2012) What the million hearts initiative means for stroke: A presedential advisory from the American Heart Association/American Stroke Association. Stroke 43: 924-928.

3. Sharma N, Cohen LG (2010) Recovery of motor function after stroke. Dev Psychol 54: 254-262.

4. Ward NS, Cohen LG (2004) Mechanisms underlying recovery of motor function after stroke. Arch Neurol 61: 1844-1848.


http://www.ncbi.nlm.nih.gov/pubmed/12878437


http://stroke.ahajournals.org/content/43/3/924



http://onlinelibrary.wiley.com/doi/10.1002/dev.20508/abstract

http://onlinelibrary.wiley.com/doi/10.1002/dev.20508/abstract



Research

Rehabilitation that incorporates virtual reality is more effective than standardrehabilitation for improving walking speed, balance and mobility after stroke:

a systematic review

Davide Corbetta a, Federico Imeri b, Roberto Gatti c

a Rehabilitation Department, San Raffaele Hospital, Milan; b Private Practice; c Laboratory of Analysis and Rehabilitation of Motor Function, Neuroscience Division,

San Raffaele Hospital, Milan, Italy

Introduction

Several studies have assessed stroke survivors’ opinions aboutthe conditions that facilitate activity and participation in dailylife.1,2 Over 70% of the respondents in these studies rated the abilityto ‘get out and about’ in the community as very important.1

However, nearly 40% of people who experience a stroke are eitherunable to walk or limited to walking within their immediateenvironment.1 Because of this limited walking ability, they cannotparticipate in community activities, which leads to a reducedquality of life.3,4 An objective of rehabilitation after stroke is toreturn the survivors to social and working activities.

The high repetition of task-oriented exercises5 has beendescribed as being important for locomotion recovery. In particu-lar, the repetition of tasks connected to locomotion has beenshown to be effective in many aspects such as improving walkingdistance and speed in people exhibiting motor deficits followingstroke.6 Virtual reality based rehabilitation (VRBR) is a relatively

recent approach that may enable simulated practice of functionaltasks at a higher dosage than traditional therapies.7,8 It consists oftechniques that allow sensory experimentation through theinteraction between humans and informatics technologies.9 Virtualreality has been defined as the ‘use of interactive simulations createdwith computer hardware and software to present users withopportunities to be engaged in environments that appear and feelsimilar to real-world objects and events’.10 The key features of allvirtual reality applications are the sense of ‘presence in’ and ‘controlover’ the simulated environment.11 The sense of ‘presence in’consists of the feeling of being in an environment, even if notphysically present in that environment; the sense of ‘control over’involves the possibility of interaction with the environment andobjects.12 These two aspects distinguish virtual reality from otherforms of visual imaging such as watching videos or television. VRBRattempts to simulate real-world activities, which may provide moreinvolving tasks when compared to standard rehabilitation. Theuse of virtual reality encourages a higher number of exercise

Journal of Physiotherapy 61 (2015) 117–124

K E Y W O R D S

Virtual reality exposure therapy

Stroke rehabilitation

Walking

Postural balance

A B S T R A C T

Question: In people after stroke, does virtual reality based rehabilitation (VRBR) improve walking speed,

balance and mobility more than the same duration of standard rehabilitation? In people after stroke,

does adding extra VRBR to standard rehabilitation improve the effects on gait, balance and mobility?

Design: Systematic review with meta-analysis of randomised trials. Participants: Adults with a clinical

diagnosis of stroke. Intervention: Eligible trials had to include one these comparisons: VRBR replacing

some or all of standard rehabilitation or VRBR used as extra rehabilitation time added to a standard

rehabilitation regimen. Outcome measures: Walking speed, balance, mobility and adverse events.

Results: In total, 15 trials involving 341 participants were included. When VRBR replaced some or all of

the standard rehabilitation, there were statistically significant benefits in walking speed (MD 0.15 m/s,

95% CI 0.10 to 0.19), balance (MD 2.1 points on the Berg Balance Scale, 95% CI 1.8 to 2.5) and mobility (MD

2.3 seconds on the Timed Up and Go test, 95% CI 1.2 to 3.4). When VRBR was added to standard

rehabilitation, mobility showed a significant benefit (0.7 seconds on the Timed Up and Go test, 95% CI

0.4 to 1.1), but insufficient evidence was found to comment about walking speed (one trial) and balance

(high heterogeneity). Conclusion: Substituting some or all of a standard rehabilitation regimen with

VRBR elicits greater benefits in walking speed, balance and mobility in people with stroke. Although the

benefits are small, the extra cost of applying virtual reality to standard rehabilitation is also small,

especially when spread over many patients in a clinic. Adding extra VRBR time to standard rehabilitation

also has some benefits; further research is needed to determine if these benefits are clinically

worthwhile. [Corbetta D, Imeri F, Gatti R (2015) Rehabilitation that incorporates virtual reality ismore effective than standard rehabilitation for improving walking speed, balance and mobilityafter stroke: a systematic review. Journal of Physiotherapy 61: 117–124]� 2015 Australian Physiotherapy Association. Published by Elsevier B.V. This is an open access article

under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

J o u rn a l o f

PHYSIOTHERAPYjournal homepage: www.e lsev ier .com/ locate / jphys

http://dx.doi.org/10.1016/j.jphys.2015.05.017

1836-9553/� 2015 Australian Physiotherapy Association. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://

creativecommons.org/licenses/by-nc-nd/4.0/).


http://crossmark.crossref.org/dialog/?doi=10.1016/j.jphys.2015.05.017&domain=pdf

http://creativecommons.org/licenses/by-nc-nd/4.0/

www.elsevier.com/locate/jphys




repetitions.13,14 It is also described as promoting motor learningthrough immediate feedback about performed tasks15 that arerelated to real-life activities16,17 such as navigation18 and roadcrossing.19,20

Previous systematic reviews have reported a moderate advan-tage obtained from VRBR on body functions of the upper limb21,22

and lower limb,23 and on activities (especially those related to thelower limb22,24,25) when compared to standard rehabilitation inpeople with stroke. A Cochrane systematic review26 published in2015 concluded that there was insufficient evidence to drawconclusions about the effectiveness of VRBR in improving gaitspeed in people with stroke. More trials have been published sincethese earlier reviews conducted their searches, allowing for meta-analyses of more outcomes and more specific comparisons.

A lot of interactive gaming consoles are available and used inrehabilitation units27,28 but virtual reality programs designedspecifically for rehabilitation purposes are still expensive and, thus,not frequently used in clinical contexts. The development of a bodyof evidence about VRBR for the functional recovery of people afterstroke may further assist the clinician in the choice of rehabilitationapproach. The aim of this work was to systematically reviewpublished studies of the efficacy of VRBR versus standard rehabili-tation in subjects presenting motor limitation following stroke.Studies performing VRBR of walking, balance and/or mobility wereincluded in the review, assuming that a post-stroke physiotherapyprogram that targets deficits in balance may be also effective inrestoring independent functional walking.29 In fact, impairedbalance seems to be related to a decreased locomotor function.30,31

This review therefore sought to answer the following questions:

1. In people after stroke, does VRBR improve walking speed,balance and mobility more than the same duration of standardrehabilitation?

2. In people after stroke, does adding extra VRBR to standardrehabilitation improve the effects on gait, balance and mobility?

Method

Identification and selection of studies

In August 2014, the Cochrane Central Register of ControlledTrials (from 1929), PubMed (from 1950), Embase (from 1980),CINAHL (from 1982) and PEDro (from 1929) databases wereelectronically searched. A modified sensitivity maximising versionof the Cochrane Highly Sensitive Search Strategy32 was combinedwith the subject-specific search in order to identify randomisedtrials that tested VRBR to train stroke survivors who had motordeficits that impaired locomotion and balance. Four key terms –‘stroke’, ‘virtual reality’, ‘walking’ and ‘postural balance’ – wereused to generate a list of search terms, which were combined into asearch strategy adapted to each database (Appendix 1 on theeAddenda).

Reference lists of identified studies and published reviews weremanually checked for additional trials. References retrieved by theelectronic search were compared for duplicate entries using the‘find duplicates’ facility of reference management software33 andwere manually crosschecked. Two review authors (DC and FI)independently selected potentially eligible articles based on thetitles and abstracts. Full-text copies of these articles were assessedagainst the inclusion criteria presented in Box 1. Disagreementswere solved by discussion, with a third reviewer (RG) consulted ifthe disagreement persisted. Eligible studies underwent dataextraction by two reviewers (DC and FI) who worked indepen-dently and used a piloted, standardised data collection form.

Assessment of characteristics of included studies

Quality

The quality of the included studies was analysed with theCochrane Collaboration’s tool for assessing risk of bias.34 The

assessment was achieved by assigning a judgment of ‘low risk’ ofbias when bias was considered unlikely to have seriously alteredthe results, ‘high risk’ of bias when the potential for bias seriouslyweakened confidence in the results, or ‘unclear risk’ when therewas some doubt about the effect of bias on the results. It wasapplied for seven specific domains: sequence generation, alloca-tion concealment, blinding of participants and personnel, blindingof outcome assessment, incomplete outcome data, selectiveoutcome reporting and ‘other issues’. Considering the nature ofthe interventions in the included studies, blinding of theparticipants and personnel would have been impractical, so onlyoutcome assessor blinding was considered.

Participants

To be eligible, studies had to have examined adults aged over18 years and with a clinical diagnosis of ischaemic or haemorrhagicstroke, as defined by the World Health Organization.35 Confirma-tion of the clinical diagnosis using imaging was not compulsory.

Intervention

Eligible studies evaluated VRBR that replaced, or was in additionto, standard rehabilitation to improve gait, balance and/or mobilityin people after stroke. If the total regimen exceeded a single session,any duration of VRBR was acceptable. The VRBR had to meet thedefinition of Schultheis 2001:

an advanced form of human-computer interface that allows the user

to ‘interact’ with and become ‘immersed’ in a computer-generated

environment in a naturalistic fashion.36

The VRBR consisted of either a single type of exercise (eg,walking while watching videos or moving in a virtually reproducedsetting) with various aims (eg, increasing walking speed, improv-ing gait and balance) or in a combination of different types ofexercises (eg, weight shifting toward the paretic side, propriocep-tive neuromuscular facilitation, or muscle strengthening). Trialsthat compared different types of VRBR without a comparison groupwere not included.

Outcome measures

The primary outcome was walking speed evaluated withobjective measures (eg, the 6-minute walk test, the 10-metre walktest, or instrumental gait analysis devices).37 The secondaryoutcomes were: measures of balance, assessed with functionalscales such as the Berg Balance Scale,38 and mobility, evaluatedwith performance measures such as the Timed Up and Go test.39

Data were extracted for the end of the intervention period and at

Box 1. Inclusion criteria

Design� Randomised or quasi-randomised controlled trial

Population� Adults (> 18 years old)

� Clinical diagnosis of stroke (ischaemic or haemorrhagic)

�No other pathological conditions affecting lower limbs (eg,

musculoskeletal disorders)

Intervention� VRBR using head mounted devices or conventional

workstation (eg, monitor, keyboard)

� Any intensity

� Duration exceeding a single treatment session

Outcomes� Walking speed

� Balance

� Mobility

Comparisons� VRBR replacing some or all standard rehabilitation

� VRBR added to standard rehabilitation versus standard

rehabilitation alone

VRBR = virtual reality based rehabilitation.

Corbetta et al: Virtual reality for stroke rehabilitation118

the longest follow-up point reported in each of the includedstudies. Any statements about adverse events were also noted.

Data analysis

Results from comparable trials were pooled using RevMansoftware.40 For the primary outcome (walking speed), data in m/swere directly obtained from each article or they were converted tom/s from the reported test description and results. For example,the velocity for performing the 6-minute walk test was calculatedby dividing the distance covered in metres by 360 seconds (totalduration of the test), or the gait speed reported as m/min in thestudy of Jaffe and colleagues41 was converted to m/s. For secondaryoutcomes, measures were similar among included studies;therefore, all results were expressed as mean differences on thesame scale. Change scores and their standard deviations were usedto compute pooled effect estimates. The pooled results from themeta-analyses were therefore expressed as weighted meandifferences (MD) with 95% CI, in the original units of themeasurement. Four authors of the included studies were contactedthrough emails for data not reported in their papers.42–45 Twoauthors42,43 replied and provided the unreported data. Theremaining unreported measures of variability were estimatedthrough the use of reported variances with an appropriatecorrection, as suggested in the Cochrane Handbook.34 In onestudy45 with non-parametric distribution of data, mean changesand their relative measures of variability were estimated with themethod proposed by Hozo et al.46 Heterogeneity was assessed byvisual inspection of the forest plot and consideration of the I2

statistic in conjunction with the chi-square test.34

Results

Flow of studies through the review

After screening the search results, 15 studies were identified forinclusion in the review.41–45,47–56 Hand searching did not identifyany additional papers. The flow of studies through the review isshown in Figure 1.

Characteristics of included studies

The included studies took place in seven countries: eight trialstook place in Korea,47–49,52–56 two in the USA,41,44 one in Taiwan,51

one in Singapore,43 one in Brazil,42 one in Spain50 and one in Italy.45

Quality

The individual items achieved by each of the includedstudies are presented in Table 1. The quality of the trials wasgood, although in three out of 15, the randomisation procedure

was unclear and half of the trials did not properly report theallocation procedure. The majority of the studies reported that theoutcome assessors were blinded. Seven studies reported with-drawals45,47–51,56 and provided the reasons for these dropouts. Alltrials were analysed on a per protocol basis. There were no markeddifferences in quality between the studies that had the sameduration of treatment in both the experimental and controlgroups41,43–45,47,49–52,54,56 and the studies that added VRBR tostandard rehabilitation in order to produce a greater amount oftreatment in the experimental group.42,48,53,55

Participants

The included studies involved 341 participants: 169 wererandomised to receive VRBR and 172 to receive standard rehabilita-tion. The mean age of the participants in the included studies rangedfrom 53 to 65 years. About 44% of the participants were female.Table 2 reports the characteristics of the participants in the includedstudies. The majority of the studies enrolled subjects who had had anepisode of ischaemic stroke more than 6 months before enrolmentinto the study. Where reported, they had preserved ability to walkwith or without an assistive device44,45,47–49,52–54 or the ability tomaintain an upright posture.42,50

Intervention

In the experimental groups of 11 studies,41,43–45,47,49–52,54,56

VRBR was integrated into or was used in place of standardrehabilitation, resulting in an equal total treatment time between

Table 1Methodological quality of included studies.

Study Random

allocation

Concealed

allocation

Assessor

blinding

Dropouts

(%)

Reasons for

withdrawals

Selective reporting

bias

Type of

analysis

Barcala et al (2013)42 LR LR LR 0 - LR P

Cho et al (2012)48 LR Unclear Unclear 8 Yes LR P

Cho et al (2013)47 LR LR LR 12 Yes LR P

Cho et al (2014)49 LR Unclear LR 6 Yes LR P

Jaffe et al (2004)41 LR HR LR 0 - Unclear P

Jung et al (2012)52 Unclear Unclear LR 0 - LR P

Kang et al (2012)56 LR LR LR < 1 Yes LR P

Kim et al (2009)53 LR Unclear LR 0 - LR P

Llorens et al (2015)50 LR LR LR 9 Yes LR P

Mirelman et al (2009)44 LR LR LR 0 - LR P

Morone et al (2014)45 LR LR LR < 1 Yes LR P

Park et al (2013)54 Unclear Unclear Unclear 0 - LR P

Rajaratnam et al (2013)43 LR Unclear LR 0 - LR P

Song et al (2014)55 Unclear Unclear Unclear 0 - LR P

Yang et al (2008)51 LR Unclear LR 16 Yes LR P

HR = high risk of bias, LR = low risk of bias, P = per protocol analysis, Unclear = unclear risk of bias.

[(Figure_1)TD$FIG]

Figure 1. Flow of studies through the review.aPapers may have been ineligible for failing to meet more than one eligibility

criterion.

Research 119

Table 2Summary of the included studies.

Study Participants Intervention Outcome measures

Barcala et al (2013)42 n = 20

Age (yr) = 64 (SD 14)

Gender = 9 M, 11 F

Exp = Conventional rehabilitation (60 min PT, 2/wk x 5 wk)

+ balance training on Nintendo WBB (30 min, 2/wk x 5 wk)

Con = Conventional rehabilitation (60 min PT, 2/wk x 5 wk)

� Balance = BBS, TUG

� Postural stability = COP oscillations

� ADL Independence = FIM

Cho et al (2012)48 n = 22

Age (yr) = 64 (SD 8)

Gender = 14 M, 8 F

Exp = Conventional rehabilitation (30 min PT + 30 min OT, 5/wk x 6 wk)

+ balance training on Nintendo WBB (30 min, 3/wk x 6 wk)

Con = Conventional rehabilitation (30 min PT + 30 min OT, 5/wk x 6 wk)


� Postural stability = PSV

Cho et al (2013)47 n = 14

Age (yr) = 65 (SD 5)

Gender = 7 M, 7 F

Exp = Conventional rehabilitation (30 min PT + 30 min OT + 20 min FES,

5/wk x 6 wk) and treadmill walking in virtual outdoor environment

(30 min, 3/wk x 6 wk)

Con = Conventional rehabilitation (30 min PT + 30 min OT + 20 min FES,

5/wk x 6 wk) and treadmill walking training (30 min, 3/wk x 6 wk)


� Gait kinematics = Spatiotemporal gait

parameters (including walking speed)

Cho et al (2014)49 n = 30

Age (yr) = 65 (SD 6)

Gender = 15 M, 15 F

Exp = Conventional rehabilitation (30 min PT + 30 min OT + 20 min FES,

5/wk x 6 wk) and treadmill walking in a virtual outdoor

environment (30 min, 3/wk x 6 wk)

Con = Conventional rehabilitation (30 min PT + 30 min OT + 20 min FES,

5/wk x 6 wk) and treadmill walking training (30 min, 3/wk x 6 wk)





Jaffe et al (2004)41 n = 20

Age (yr) = 61 (SD 10)

Gender = 12 M, 8 F

Exp = Stepping over virtual objects on treadmill (60 min, 3/wk x 2 wk)

Con = Stepping over real foam objects in a hallway (60 min, 3/wk x 2 wk)

� Gait endurance = 6MWT



�Others = Obstacle clearance test, Balance test

� Adverse events

Jung et al (2012)52 n = 21

Age (yr) = 62 (SD 7)

Gender = 13 M, 8 F

Exp = Treadmill walking in a virtual outdoor environment (30 min,

5/wk x 3 wk)

Con = Treadmill walking training (30 min, 5/wk x 3 wk)

� Balance = TUG

� Balance self-efficacy = ABC scale

Kang et al (2012)56 n = 30

Age (yr) = 56 (SD 7)

Gender = 16 M, 14 F

Exp = Conventional rehabilitation (PT 5/wk x 4 wk) + treadmill walking

with optic flow (30 min, 3/wk x 4 wk)

Con 1 = Conventional rehabilitation (PT 5/wk x 4 wk) + treadmill training

(30 min, 3/wk x 4 wk)

Con 2 = Conventional rehabilitation (PT 5/wk x 4 wk) + stretching added

ROM exercises (30 min, 3/wk x 4 wk)

� Balance = TUG

� Walking speed = 10MWT


� Others = FRT

Kim et al (2009)53 n = 24

Age (yr) = 53 (SD 9)

Gender = 13 M, 11 F

Exp = Conventional rehabilitation (40 min PT, 4/wk x 4 wk) + VR exercises

for balance and stepping skills (30 min, 4/wk x 4 wk)


� Balance = BBS





� Others = MMAS

Llorens et al (2015)50 n = 20

Age (yr) = 57 (SD 11)

Gender = 9 M, 11 F

Exp = Conventional rehabilitation (30 min PT, 5/wk x 4 wk) + stepping task

in a 3D virtual environment (30 min, 5/wk x 4 wk)


� Balance = BBS, Tinetti POMA, BBA


Mirelman et al (2009)44 n = 18

Age (yr) = 61 (SD 9)

Gender = 15 M, 3 F

Exp = Robot training for foot movements in a virtual environment

(60 min, 3/wk x 4 wk)

Con = Robot training for foot movements without a virtual environment

(60 min, 3/wk x 4 wk)

� Balance = BBS




� Others = FMA (lower extremity)

Follow-up = 3 mth

Morone et al (2014)45 n = 47

Age (yr) = 60 (SD 10)

Gender = Unreported

Exp = Conventional rehabilitation (40 min PT, 2 times/day x 4 wk)

+ Nintendo WBB (20 min, 3/wk x 4 wk)

Con = Conventional rehabilitation (40 min PT, 2 times/day x 4 wk)

+ balance therapy (20 min, 3/wk x 4 wk)

� Balance = BBS


� ADL Independence = BI

� Others = FAC

Park et al (2013)54 n = 16

Age (yr) = 48 (SD 8)

Gender = 11 M, 5 F

Exp = Conventional rehabilitation (60 min PT, 5/wk x 4 wk) + VR-based

postural control exercises (30 min, 3/wk x 4 wk)

Con = Two administrations of conventional rehabilitation (60 min PT,

5/wk x 4 wk) + (30 PT min, 3/wk x 4 wk)




� Follow-up = 1 mth

Rajaratnam et al (2013)43 n = 19

Age (yr) = 62 (SD 9)

Gender = 7 M, 12 F

Exp = Conventional rehabilitation (40 min PT, 15 sessions) + balance

training on Nintendo WBB or Microsoft Kinect (20 min, 15 sessions)

Con = Conventional rehabilitation (60 min PT, 15 sessions)


� Postural stability = COP oscillations

� ADL Independence = MBI

Others = FRT

Song et al (2014)55 n = 20

Age (yr) = 63 (SD 14)

Gender = 11 M, 9 F

Exp = Conventional rehabilitation (25 min PT, 5/wk x 3 wk) + VR-based

balance training (25 min, 3/wk x 3 wk)


� Balance = BBS

� Others = FI, SI, WDI

Yang et al (2008)51 n = 20

Age (yr) = 58 (SD 11)

Gender = 10 M, 10 F

Exp = Treadmill walking in virtual outdoor environment (20 min,

3/wk x 3 wk)

Con = Treadmill training simulating stepping obstacles (20 min,

3/wk x 3 wk)

� Gait kinematics = walking speed

� Others = ABC, WAQ, CWT

� Follow-up = 1 mth

10MWT = 10-metre Walk Test, 6MWT = 6-minute Walk Test, ABC = Activities-specific Balance Confidence, ADL = activities of daily living, BBA = Brunel Balance Assessment,

BBS = Berg Balance Scale, BI = Barthel Index, Con = control group, COP = centre of pressure, CWT = Community Walk Test, Exp = experimental group, F = female, FES = functional

electrical stimulation, FI = Falling Index, FIM = Functional Independence Measure, FMA = Fugl-Meyer Assessment, FRT = Functional Reach Test, M = male, MBI = Barthel Index,

MMAS = Modified Motor Assessment Scale, OT = occupational therapy, POMA = Performance-Oriented Mobility Assessment, PSV = Postural Sway Velocity, ROM = range

of motion, SI = Stability Index, TUG = Timed Up and Go, WAQ = Walking Ability Questionnaire, FAC = Functional Ambulatory Category, WDI = Weight Distribution Index,

PT = physiotherapy, VR = virtual reality, WBB = Wii Balance Board.


the experimental and control groups. Among these studies, theinterfaces most frequently used for walking rehabilitation werevirtual reality treadmill training systems.41,47,49,51,52,56 Someconsisted of a treadmill and a wide screen that projected a real-world video recording in order to reproduce an immersive virtualoutdoor environment;47,49,51 others used a head-mounted deviceinstead of the monitor.41,52,56 One study used the head-mounteddevice without a treadmill.54 For balance training, one study43

used Microsoft Xbox 360 Kinecta, one study45 used Nintendo WiiFitb and one study50 used an audio-visual system combined with amotion-tracking system in order to immerse participants in a 3Dvirtual environment. In the study of Mirelman and colleagues,44 arobotic virtual reality device was used for training movement ofthe lower extremity.

In four studies,42,48,53,55 VRBR was added to standard rehabili-tation, resulting in a greater amount of treatment time in theexperimental group. Two of these studies53,55 used the IREX1c

virtual reality system for rehabilitation of walking and balance. Itconsisted of a television monitor, a video camera, cyber gloves andvirtual objects, scenes and a large screen. The other two studiesonly trained balance by using the Wii Fit balance program.42,48

Frequency of interventions varied from 242 to 641 days a weekand lasted from 241 to 6 weeks.47–49 The duration of each trainingsession ranged from 20 minutes51 to 1 hour.41–44,50

Outcome

Nine studies measured locomotor function: five used the 10-metre walk test,45,50,53,54,56 two used the 6-minute walk test41,44

and two measured gait velocity.47,51 Balance was assessed usingthe Berg Balance Scale in nine studies42,43,45,47–50,53,55 and mobilitywas assessed using the Timed Up and Go test in sevenstudies.42,43,47–49,52,56 Outcomes were assessed immediately afterthe intervention. Only four studies included follow-up evaluationsat 151,54 or 344,45 months after training.

Does VRBR improve outcomes more than the same duration ofstandard rehabilitation?

Walking speed

Walking speed was obtained from walking measures reported inseven studies41,44,47,50,51,54,56 and converted to the same unit ofmeasurement(m/s).Thesestudies reporteddataon138 participants,65 of whom received VRBR. Replacing some or all of the standardrehabilitation with VRBR (for the same total treatment time)significantly improved walking speed, with a mean differenceof 0.15 m/s (95% CI 0.10 to 0.19), as presented in Figure 2.

See Figure 3 on the eAddenda for a more detailed forest plot. Noimportant statistical heterogeneity was observed (I2 = 26%).

Three studies measured walking speed beyond the end of theintervention period.44,51,54 These studies reported data on54 participants, 28 of whom received VRBR. The effect of theVRBR was well maintained for 1 to 3 months after the end of theintervention period, with a mean difference of 0.12 m/s (95% CI0.03 to 0.20), as presented in Figure 4. See Figure 5 on the eAddendafor a more detailed forest plot. No statistical heterogeneity wasobserved (I2 = 0%).

In addition to the studies that could be meta-analysed, Moroneand colleagues45 measured gait speed over 10 m but only reportedpercentage improvement. They reported that at the end of the4-week intervention period gait speed improved by 35% in theexperimental group and by 27% in the control group. One monthafter ceasing the intervention each group improved a further 6%.Although these differences were not statistically significant, theyare in the same direction and of a similar magnitude to the meta-analysed studies of this review.

Balance

Balance was assessed with the Berg Balance Scale in fivestudies.43,45,47,49,50 These studies reported data on 130 participants,67 of whom received VRBR. Replacing some or all of the standardrehabilitation with VRBR (for the same total treatment time)significantly improved balance, with a mean difference of2.1 points on the 0-to-56-point Berg Balance Scale (95% CI1.8 to 2.5), as presented in Figure 6. See Figure 7 on the eAddendafor a more detailed forest plot. No statistical heterogeneity wasobserved (I2 = 0%).

Mobility

Mobility was assessed using the Timed Up and Go test in fivestudies.43,47,49,52,56 These studies reported data on 114 participants,53 of whom received VRBR. Replacing some or all of the standard[(Figure_6)TD$FIG]

2

Study

Cho47

Cho49

Lloréns50

Morone45

Rajaratnam43

Pooled

MD (95% CI)Random

Favours SR (points) Favours VRBR

−2−4 0 4

Figure 6. Weighted mean differences (95% CI) of the effect of substituting some or

all of standard rehabilitation (SR) with virtual reality based rehabilitation (VRBR) on

the Berg Balance Scale score (0 to 56 points), pooling data from five trials (n = 130).

[(Figure_2)TD$FIG]

−0.25−0.50 0 0.500.25

Study

Cho47

Jaffe41

Kang56

Lloréns50

Mirelman44

Park54

Yang51

Pooled

MD (95% CI)Random

Favours SR (m/s) Favours VRBR

Figure 2. Weighted mean differences (95% CI) of the effect immediately after

intervention of substituting some or all of standard rehabilitation (SR) with virtual

reality based rehabilitation (VRBR) on walking speed, pooling data from seven trials

(n = 138).

[(Figure_4)TD$FIG]

0.1

Study

Mirelman44

Park54

Yang51

Pooled

MD (95% CI)Random

Favours SR (m/s) Favours VRBR

−0.1−0.2 0 0.2

Figure 4. Weighted mean differences (95% CI) of the effect beyond the end of the

intervention period of substituting some or all of standard rehabilitation (SR) with

virtual reality based rehabilitation (VRBR) on walking speed, pooling data from

three trials (n = 54).

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rehabilitation with VRBR (for the same total treatment time)significantly improved mobility, with a mean difference of2.3 seconds on the Timed Up and Go test (95% CI 1.2 to 3.4), aspresented in Figure 8. See Figure 9 on the eAddenda for a moredetailed forest plot.

Substantial statistical heterogeneity was observed (I2 = 84%),which was mainly due to the magnitude of the effect estimatedfrom the studies of Kang et al56 and Rajaratnam et al.43 Performinga sensitivity analysis, through the exclusion of these studies fromthe overall estimation, the level of heterogeneity became accept-able (I2 = 0%) with a similar estimate of 1.3 (95% CI 1.0 to 1.7). Theanalysis is presented in Appendix 2 on the eAddenda.

Adverse events

One of the study reports included a statement about adverseevents, stating that there were no falls and no undue cardiovascu-lar responses in either group.41 However, some of the other studyreports included statements that implied that adverse eventswould have been mentioned if they had occurred. For example,Yang et al51 and Kang et al56 stated that a staff member stayedclose to each participant during the intervention in order toprevent falls.

Does adding extra VRBR to standard rehabilitation improveoutcomes?

Walking speed

One study, involving 42 participants, assessed the effect of extraVRBR on walking speed.53 Although the group that received theextra VRBR increased walking speed by an average of 0.21 m/smore than the standard rehabilitation group, this was notstatistically significant (95% CI –0.23 to 0.65). This study did notassess outcomes beyond the intervention period.

Balance

Balance was assessed with the Berg Balance Scale in fourstudies.42,48,53,55 These studies reported data on 86 participants,43 of whom received the extra VRBR. These studies were tooheterogeneous to be pooled (I2 = 97%), as presented in Figure 10. SeeFigure 11 on the eAddenda for a more detailed forest plot.

Mobility

Mobility was assessed using the Timed Up and Go test in twostudies.42,48 These studies reported data on 42 participants, 21 ofwhom received the extra VRBR. The group that received the extraVRBR improved their mobility on the Timed Up and Go testsignificantly more than the standard rehabilitation group, with amean difference of 0.7 seconds (95% CI 0.4 to 1.1), as presented inFigure 12. See Figure 13 on the eAddenda for a more detailed forestplot. No statistical heterogeneity was observed (I2 = 0%).

Adverse events

None of the reports of the included studies made an explicitstatement about adverse events, but some implied that no adverseevents occurred. For example, Cho and colleagues stated that a staffmember stayed close to each participant during the rehabilitationin order to prevent falls.48

Discussion

The meta-analyses in this systematic review identified somebeneficial effects of VRBR on walking speed, balance and mobilityoutcomes in stroke survivors. These analyses are based on 15 eligibletrials with a total of 341 participants, which exceeds the amount ofdata relating to clinical mobility outcomes that has been reported inpast systematic reviews on VRBR after stroke.21–26,57 Also, thisreview conducted meta-analyses for clinical mobility outcomeswith separate meta-analyses depending on whether the VRBR wassubstituted for, or in addition to, standard rehabilitation. Only one ofthe past reviews conducted meta-analyses with this distinction, butit only analysed walking speed, not balance or mobility.57 Therefore,while the results of this new review are consistent with the generalfinding of the past reviews (ie, that VRBR appears to be beneficial forpeople with stroke), some important new insights have beenobtained.

The meta-analyses of those trials where the VRBR wassubstituted for some or all of the standard rehabilitation (to givethe same total treatment time) showed significant improvementsin walking speed, balance and mobility. These results indicate that,for a given treatment time, VRBR is more beneficial than standardrehabilitation. These findings predict that even greater effectswould be seen in the remaining analyses (ie, those where the VRBRwas provided as extra treatment time added to a standardrehabilitation regimen). However, this was not clearly observed inthese outcomes for several reasons. For walking speed, only onestudy53 analysed the effect of additional VRBR. The mean estimate(0.21 m/s) was greater than the effect seen in the earlier meta-analysis (0.15 m/s, Figure 2), but the result was insignificant. Thewide confidence interval (95% CI –0.23 to 0.65) means that thepotential for a strong benefit in walking speed from additional

[(Figure_12)TD$FIG]

0.5

Study

Barcala42

Cho48

Pooled

MD (95% CI)Random

Favours SR (s) Favours VRBR

−0.5−1 0 1

Figure 12. Weighted mean differences (95% CI) of the effect of adding extra virtual

reality based rehabilitation (VRBR) to standard rehabilitation (SR) on the Timed Up

and Go test, pooling data from two trials (n = 42).

[(Figure_8)TD$FIG]

5

Study

Cho47

Cho49

Jung52

Kang56

Rajaratnam43

Pooled

MD (95% CI)Random

Favours SR (s) Favours VRBR

−5−10 0 10

Figure 8. Weighted mean differences (95% CI) of the effect of substituting some or

all of standard rehabilitation (SR) with virtual reality based rehabilitation (VRBR) on

the Timed Up and Go test, pooling data from five trials (n = 114).

[(Figure_10)TD$FIG]

2

Study

Barcala42

Cho48

Kim53

Song55

MD (95% CI)Random

Favours SR (points) Favours VRBR

−2−4 40

Figure 10. Mean differences (95% CI) of the effect of adding extra virtual reality

based rehabilitation (VRBR) to standard rehabilitation (SR) on the Berg Balance

Scale score (0 to 56 points), with no pooling due to heterogeneity (n = 86).


VRBR has not yet been excluded; therefore, further research couldhelp to refine this estimate. Although four studies reported data forbalance, the studies were too heterogeneous to be pooled. Whenmobility was analysed, a significant benefit was observed.However, the effect (0.7 seconds on the Timed Up and Go test,Figure 12) was smaller than the effect seen in the earlier meta-analysis (2.3 seconds, Figure 8). This effect may also be too small tobe considered clinically worthwhile by many patients; given thatthe time spent doing the additional VRBR in the included studieswas 30 minutes, two to three times per week, for 5 to 6 weeks.

From the analysis of the included studies, it may not be possibleto generalise about the efficacy of VRBR in motor recovery of thefull range of people after stroke. First of all, most of the studies onlyrecruited participants with mild motor impairment, as wasdemonstrated by their ability to walk independently and by thehigh Berg Balance Scale scores. Furthermore, almost all of thestudies recruited people who had a stroke more than 6 monthsbefore study enrolment, with only three studies43,45,55 evaluatingthe VRBR in acute stroke patients.

An open question is whether the changes induced by VRBR areclinically relevant. In previous studies, Flansbjer and collea-gues58,59 reported 95% CIs of the smallest real difference as –0.15 to 0.25m/s for comfortable walking speed, –3.4 to 4.9 pointsfor the Berg Balance Scale and –3.8 to 2.6 seconds for the Timed Upand Go Test for individuals with chronic hemiparesis subsequentto stroke. Even though the smallest real difference is not aninstrument to define clinical relevance, the fact that the notedeffects were smaller than the smallest real difference limits theability to conclude that these were real improvements.

The effect of VRBR on walking speed would seem to bemaintained from 1 month51,54 to 3 months44 of follow-up. Theoptimal frequency, intensity, time and type of VRBR are stillunclear. Finally, no adverse events were reported in the includedstudies, suggesting that VRBR can be considered a safe treatmentfor subjects after stroke.

The effects obtained by VRBR could be due to the multisensory(visual and auditory) feedback provided by virtual reality systemsand to the influence of motivational aspects on motor perfor-mance.25,60,61 These sensory information allow the central nervoussystem to better control position and orientation of body segmentsadapting to the complex external environment.62 Moreover, Youet al63 suggested that treatment using virtual reality facilitatescortical reorganisation. The VRBR settings were also used toreproduce training activities that closely reproduce real-worldtasks, which have been shown to maximise training effects.64 Thisrepresents one of the most important features of exercisesproposed in neurorehabilitation; they must be highly repetitiveand task oriented in order to facilitate the recovery of functions andactivities.65

The authors of several of the eligible studies42,47,49,51,53

included statements that the VRBR was motivating and moreinvolving than standard rehabilitation, although none of themdirectly assessed the attitude of participants toward VRBR.

Although this meta-analysis suggests that VRBR improveswalking speed, balance and mobility in people with stroke morethan the same time spent doing standard rehabilitation, furtherrandomised trials with large sample sizes are encouraged. Theadditional data would help to confirm these results and to improvethe precision of the estimates. Further trials that apply the VRBR asextra time added to a standard rehabilitation regimen will help toprovide estimates specifically about this use, where the effects onwalking speed and balance are unclear. Finally, further trials couldalso help to determine the optimal frequency, intensity, time andtype of VRBR, as well as identifying what may be causing some ofthe heterogeneity seen in this review.

In conclusion, VRBR appears to produce greater benefits inwalking speed, balance and mobility for a given amount ofrehabilitation time than standard rehabilitation after stroke. VRBRdid not appear to increase the likelihood of adverse events and ithas been reported to increase motivation and involvement of

people undergoing rehabilitation. Therefore, it appears to bejustified to propose VRBR to people who have experienced a strokein order to promote their recovery of walking speed, balance andmobility.

What is already known on this topic: Problems withwalking speed, balance and mobility are common after stroke,but high repetition of task-oriented exercises can improvethese sequelae. Virtual reality-based rehabilitation enablessimulated practice of functional tasks, with moderate benefitson some upper and lower limb tasks over standard rehabilita-tion for people with stroke.What this study adds: Substituting some or all of a standardrehabilitation regimen with virtual reality-based rehabilitationelicits greater benefits in walking speed, balance and mobilityin stroke patients.

eAddenda: Figures 3, 5, 7, 9, 11 and 13 and Appendices 1 and2 can be found online at doi:10.1016/j.jphys.2015.05.017.

Footnotes: a Microsoft Xbox 360 Kinect, Microsoft Co.,Redmond, WA, USA, b Nintendo Wii Fit, Nintendo Inc., Japan,c IREX1, GestureTek, Toronto, Canada.

Ethics approval: Not applicable.Competing interests: Nil.Source(s) of support: Nil.Acknowledgements: We wish to acknowledge Dr Luciana

Barcala and Dr Bala Rajaratnam for providing unpublished data.We thank Francesca Nicastro for the language consult.

Provenance: Not invited. Peer-reviewed.Correspondence: Davide Corbetta, Rehabilitation Department,

San Raffaele Hospital, Milan, Italy. Email: [email protected]

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mailto:[email protected]

http://refhub.elsevier.com/S1836-9553(15)00056-9/sbref0330











































“This course was developed and edited from the document: Non-immersive Virtual Reality

for Fine Motor Rehabilitation of Functional Activities in Individuals with Chronic Stroke: A

Review - LeBlanc S, Paquin K, Carr K, Horton S (2013), International Journal of Aging Science

(1: 105. doi:10.4172/jasc.1000105), used under the Creative Commons Attribution License.”

“This course was developed and edited from the document: ) Rehabilitation that Incorporates

Virtual Reality is More Effective than Standard Rehabilitation for Improving Walking Speed, Balance

and Mobility After Stroke: A Systematic Review - Corbetta D, Imeri F, Gatti R (2015), Journal of

Physiotherapy (61: 117–124 http://dx.doi.org/10.1016/j.jphys.2015.05.017), used under the Creative

Commons Attribution License.”


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