Multiple game based rehabilitation platform instead of intensified conventional balance training in patients with stroke: pilot study

Background: People who survive a stroke usually suffer for moderate to severe movement disorders such as uncontrollable movements of the limb, posture and balance disorders. An intensive and repetitive physiotherapy and balance training are often a key to functional restoration of movements. Recently modern rehabilitation centers have offered virtual reality supported balance training with exergames in addition to the conventional therapy. However, the choice of the appropriate exergame is still not straightforward. Methods: We designed a randomized pilot study investigating how different types of balance training in addition to the physiotherapy program influence on functional outcomes. 20 eligible participants were randomized into 2 groups; exergaming vs conventional balance training. Multiple-game platform with exergames supporting single leg exercises, weight shifting, balancing and standing up and equivalent conventional physiotherapy exercises were used. Center of pressure was monitored during exergaming and clinical impact was evaluated with the Four Square Step Test (FSST), Timed Up & Go, 10m Walk Test (10MWT), Romberg, Sharpened Romberg, Clinical Test for Sensory Interaction in Balance in both groups. Statistical tests were used to find statistically significant (p < 0.05) differences and Cohen’s U3 test to examine the effect sizes. Results: Participants of both groups demonstrated substantively and statistically significant improvements of functional balance, in particular the exergaming group (FSST p = 0.009, U3 = 0.9 and 10MWT p = 0.008, U3 = 0.9). . However, significant differences between the groups were found only in tests with eyes closed, Sharpened Romberg test (p = 0.05) and standing on the right leg (p = 0.035). We found a decrease of center of pressure area for up to 20% in the exergaming group. Conclusions: In the exergaming group the participants achieved improved functional balance that could be well targeted by the selection of games and objectively evaluated. The modern approach had a great potential by choosing

the appropriate game to target the exercise, but the low statistical power may hinder the equivalence of both additional balance training methods. However, the exergaming provided independent balance training, also feasible without physiotherapist's strenuous work that may be crucial for future home or telerehabilitation services. Background 1.1 Motor function rehabilitation after stroke Cerebrovascular accident or stroke is a consequence of blood supply interruption in some parts of the brain due to the blood spill or blood block in the blood vessel by a clot. People having a stroke are affected cognitively and physically and deprived of daily living functions. If the stroke is very severe, the person may die immediately, if not, consequences depends on which part of the brain is injured and how severe was the stroke. However, nearly 80% of survivors of nearly 15 million strokes worldwide each year (WHO) suffer for motor function impairment and are in need for comprehensive motor rehabilitation to get back to their everyday life routine (1). For successful motor rehabilitation an intensive exercises are required (2) that is often limited due to time constraints and lack of therapists even in the top rehabilitation clinics. A temporary solution is to prepare the patients for an additional home exercise, which is in most cases unsuccessful due to the lack of motivation. Those patients rarely meet the prescribed home rehabilitation regimens (3) and are advised to visit the outpatient clinic. Clinical studies suggested at least 3 hours of timed exercises per week (4). The authors agreed that duration and intensity of exercises would have been crucial for optimal rehabilitation outcomes, no matter if rehabilitation was carried out in clinical or home environment.
Both rehabilitation environments, clinical and home, have one crucial element in common, i.e. patient's motivation. Several researchers have developed rehabilitation games, also in virtual reality, to increase the motivation of the patients and engage them in the motor rehabilitation more intensively (5). The main focus of rehabilitation games may be attracting patients' attention and motivating them to achieve higher score, while the virtual reality based rehabilitation offers interactive simulated environments. The users are engaged in these environments that could be similar to the real world or imaginary objects and events. The rehabilitation games are often controlled by sensors, recently contactless motion tracking sensors (Microsoft Kinect, Leapmotion, etc) or force plates (Wii Balance Board, AMTI, etc) that serve also as an assessment devices. Patients with severe stroke may often need a passive or active rehabilitation robot providing upper limb (6), (7) or lower limb support (8), (9), (10).

Exergaming in balance training
Balance and posture are considered complex motor and cognitive functions depending on various factors, such as muscle power, mobility, and sensory information from musculoskeletal system, visual and vestibular systems. Cognitive and emotional factors should also not be neglected (11). Cerebrovascular accident or stroke often affects balance, posture and mobility, increased risk of falls (1) and limited daily living activities.
Clinical findings emphasize the importance of large number of regular repetitions of functional movements to achieve neuroplastic changes in the brain, which would result in functional improvement of motor functions (2), (3). However, the conventional physiotherapy is often limited in providing large number of repetitions due to the limited time available for each patient, limited number of skilled professionals or other related organizational problems (12), (4). In last decade researchers have proposed exergaming and virtual reality (VR) supported rehabilitation as a tool to increase repeatability and controllability of the physiotherapeutic processes.
The literature review provides a long list of publications emphasizing the importance and advantages of using VR and exergames in the rehabilitation. The VR and exergames provide variety of options for eliciting the maximum voluntary activity of the patient, like accurate task repetitions, frequency, intensity, changes of virtual environments and gradual increase of task complexity (13 to the server to enable the physiotherapist a remote insight into the patient's performance and required changes of the telerehabilitation program.

Objectives of the paper
Previous studies demonstrated that implementing rehabilitation games into the process of physiotherapy can be not only effective or provide good clinical experience, but also scientific studies provided clinically evidences (15). Most of the studies were intended for the controlled clinical settings and the entire process was carried out by the medical professional, often a physiotherapist. The objective of our paper was to demonstrate that using specific rehabilitation games based on Gentile's taxonomy for additional balance training could be as successful as conventional physiotherapy and would allow targeting specific neuromotor control exercises. The physiotherapist was present only to supervise the process, ensure safety for the patient and to prevent any event that could potentially lead to an accident. We expect that motivation and independent use of exergames may in the future contribute to the prolonged rehabilitation at patient's home, while the therapist will remain as a consultant. Hereby we raise the following research hypothesis:  (Figure 1). The feet and the legs were held apart as at normal upright posture. After the start of the REWIRE platform, the system had been configured and the participant/physiotherapist was able to choose a game and set up a difficulty level and duration time.
The games were designed to follow the modified Gentile's taxonomy of motor skill (17).

Participants
For the study 30 acute and subacute stroke survivors were recruited, but only 20 were eligible ( Figure 3). They met the inclusion criteria defined by the responsible physician: 1.
first ischemic or hemorrhagic stroke, 2. first admission to rehabilitation programs, 3.   COP displacement area depended on the balance/sway performance of the participant.
Balance disorders and instability resulted in wider and larger COP area ( Figure 4). The COP area was estimated by the 95% confidence ellipse (19). The computation was done by   Mauchly's test of sphericity (27) indicated that the assumption of sphericity in the data had been violated, χ2 = 45.599, p < 10 -4 . Therefore the Greenhouse-Geisser correction was applied to the degrees of freedom (df) for the F-distribution (e = 0.456). The effects within subjects were calculated with the repeated measures ANOVA after the corrections had been made. Corrections had no effect on sum of squares or the F, but affected df and the p-value. We found the changes in COP area ( Figure 5) thought the sessions statistically insignificant (p = 0.222). Additionally the interaction effect between time and the exergame was also found insignificant (p = 0.114). However, the Tukey HSD post-hoc test found statistically significant differences between the exergames AnimalHurdler and FruitCatcher, AnimalHurdler and HorseRider (p < 0.003). But statistically insignificant differences were found in the mean COP area between the exergames FruitCatcher and HorseRider (p = 0.088).

Success in gaming
The total points achieved in particular exergames were not comparable to each other.
Comparison of total points achieved was carried out between the sessions for each particular exergame.
The overview of total points achieved in the AnimalHurdler shows that the participants successfully accomplished the game in the last 2 sessions with 26% higher score ( Figure   6). The detailed analysis of the median and interquartile range demonstrated large variation of the results (the score range 100-3500, p = 0.306), however, the median values showed higher score at the end () of the exergaming. In the 4 th session we have noticed sample skewness.
In the FruitCatcher exergame the participants achieved 8%, 10% higher mean score at the 4 th (mean 2438 points) and 5 th session (mean 2460 points, p = 0.458), respectively. The analysis of the median values (Figure 6), the distribution of the score and interquartile range demonstrated that participants had been able to accomplish the game successfully with equal score even at the session 2 (mean 2316 point) and 3 (mean 2303 points). The outcomes of the FruitCatcher game for the session 1 were corrupt or missing for 3 participants, thus we considered the score for this session invalid.
On the other hand the results of the HorseRider exergame show that participants were able to achieve high score even at the session 1 (mean 3071 points) or at the session 4 (mean 3060 points). The median value of the total points dropped at the sessions 2 and 3 and the 1.5 x interquartile range demonstrated a large variation in total game score, particularly in session 3. However, the mean values at HorseRider game slightly dropped at the session 2 (mean 2832 points) and was higher in the session 3 (mean 2945 points) and session 5 (mean 2990 points, p = 0.268).

Clinical outcomes
The balance, postural and mobility tests FSST, TUG and MWT demonstrated functional improvements (  (Table 3) and time effect was statistically insignificant (p > 0.369, c 2 < 6.53).

Differences between the groups
The differences in age, time since stroke, affected side and MMSE were statistically analyzed for 20 participants randomized into 2 groups. The variances were assumed equal (Leven's Test) for gender and time since stroke variables, therefore t-test assuming unequal variances was used. We found minor and statistically insignificant differences between the two groups of participants ( Table 4).
Despite the gaming group demonstrated significant progress in motor and balance tests MWT (p = 0.008) and FSST (p = 0.009), but not also gait test TUG (p = 0.092), the outcomes were not significantly different (p > 0.05, Man-Whitney U Test) from the controlgroup in any of these tests (Figure 7).
Standing on the right leg with eyes closed (STORL EC) demonstrated significant differences between the groups (p = 0.035, Man-Whitney U Test, Figure 8) These findings were in line with our expectations and previously published studies suggesting that the COP area displacement had been positively correlated to the balance and gait parameters (28). The studies also reported on results that were correlated to the muscle strength, gait performance, balance, postural control and stability and their improvement with the reduction of COP area after the rehabilitation/physiotherapy in patients diagnosed with stroke (29) and appeared to be significantly different in persons diagnosed with stroke and healthy persons (30).
The attractiveness of the exergames plays an important role in rehabilitation outcomes (31) therefore the achieved game score is not a negligible information. The achieved mean game scores at FruitCatcher and AnimalHurdler were higher at the end than at 1 st or 2 nd session indicating that participants' effort was still present. The mean score with HorseRunner was rather fluctuating. This information was not necessarily directly related to the improvement of balance abilities, but rather presented an intrinsic motivation factor for the participants (32).

Conventional physiotherapy group
The provided balance training program contributed to the statistically significant reported that the main changes in FSST were noticed from the baseline to the second week and only minor changes were reported from week 2 to week 4. The FSST was considered a dynamic balance test that could successfully assess changes during balance training in stroke population and provide ancillary information about daily living activities.
Participant finishing the test in more than 12s were classified in a group with increased risk for falls (20). According to these criteria both participating groups were considered fallers before the additional balance training. However, only the exergaming group achieved the mean score of 10.24s, making the group for non-fallers. Besides, the change was considered statistically significant (p = 0.009). TUG and MWT both demonstrated clinically proven improvements, but no statistical difference between both approaches was found.
The major advantage of the exergaming approach was the access to the objective, measurable information like the COP. The COP area displacement was reported to be in correlation with the clinically proven tests for balance and posture evaluation (28) and furthermore we even found differences between the applied exergames. Therefore the appropriate choice of the exergame may help targeting specific balance or postural disorder.
The gaming group found the additional balance training challenging according to the achieved score which is in line with the findings of Hung et al (31) who reported on importance of game diversity and fun.
We have demonstrated that exergaming can be equivalent to conventional intensive balance training in the additional rehabilitation program. Furthermore, valuable results were demonstrated by FSST and tests with closed eyes. So far we do not expect that virtual reality based rehabilitation is far more effective than conventional rehabilitation (15), but in our opinion we could achieve promising results with the additional balance and mobility training without replacing any existing clinical method and possibly extend the rehabilitation period for a larger stroke population, if they can perform some exercises at home.

Limitations of the study and future work
The objective of the study was additional balance training in the rehabilitation program based on multi-exergaming that may replace the additional balance training in patients recovering from stroke. We measured the kinematics of the whole body with the camera and COP with the low-cost force plate. The COP could be assessed also in the control group to make the results also objectively comparable, however the clinical exercises for balance training would have provided different, directly incomparable data. The solution might have been development of task specific tests that would be equal for both groups.
Despite the games score was a good indicator of participants effort, we could have applied also the intrinsic motivation inventory (36) to both groups.
On the other hand the clinical tests demonstrated much higher variance than expected for the planned statistical power (0.8). The recruited sample size would have been large enough to cover the objective assessments, but unfortunately not all patients were eligible for the study. The small sample size caused violation of the assumption of sphericity (Mauchly's test) and statistical degrees of freedom were corrected in the study.
We see a small sample size as a limiting factor to assure the sphericity of the data and also for decreasing the statistical power to the analysis of the clinical tests. We may suggest that the balance training was equivalent in both groups as reported by the literature (15) and rather medium to large effect sizes were found. But further randomized clinical trials are needed to promote exergaming. Particularly if the evaluation tool is intended for objective evaluation of the remote (tele)rehabilitation.

Conclusions
In the study advantages of the multi-exergames targeting balance, posture, single leg standing, weight shifting or simply just muscles strengthening by sit-to-stand exercise were demonstrated. There has been decades of scientific reporting that exergaming can contribute to the improvement of fine and gross motor skills in patients diagnosed with stroke. The contemporary approach provides non-negligible advantages over additional conventional balance training in terms of objective assessment and more targeted balance and posture disorders. .
Additionally the study showed that significant differences were found only in clinical tests closed eyes and FSST. This led us to the conclusions that both approaches could be equivalent in terms of effectiveness, however, the exergaming may require less strenuous work and physiotherapist's interventions and has a potential for telerehabilitation (37).
We suggest that future studies should take into account also the motivation factor of the participants and examine whether the exergame difficulty level would affect the voluntary contribution of each individual and how such approach could also work out in home environment.

Declarations
Ethics approval and consent to participate   All games were intended for balance and posture, but Animal Hurdler game (1) also for weight shift and single leg standing, Fruit Catcher game (2) also for weight shift and steps and The Horse Runner game (3) also for sit-to-stand exercise. The 95% of the area covered by the ellipse was determined by calculating the eigenvectors. and Horse runner (HR) games in terms of COP area (p = 0.088), but only between the Animal hurdler (AH) and other two (p < 0.003).

Figure 6
Points achieved in each exergame FruitCatcher (FC), AnimalHurdler (AH) and Horse Runner (HR). Mean values show that participants performed better at the last and pre-last sessions with the FC and AH games. However, the median values and the interquartile ranges revealed that despite of the noticeable progress in AH we had many participants with low score (p > 0.05).