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Background: Use of exergames can complement conventional therapy and increase the amount and intensity of visuospatial neglect (VSN) training. A series of 9 exergames—games based on therapeutic principles—aimed at improving exploration of the neglected space for patients with VSN symptoms poststroke was developed and tested for its feasibility. Objectives: The goal was to determine the feasibility of the exergames with minimal supervision in terms of (1) implementation of the intervention, including adherence, attrition and safety, and (2) limited efficacy testing, aiming to document possible effects on VSN symptoms in a case series of patients early poststroke. Methods: A total of 7 patients attended the 3-week exergames training program on a daily basis. Adherence of the patients was documented in a training diary. For attrition, the number of participants lost during the intervention was registered. Any adverse events related to the exergames intervention were noted to document safety. Changes in cognitive and spatial exploration skills were measured with the Zürich Maxi Mental Status Inventory and the Neglect Test. Additionally, we developed an Eye Tracker Neglect Test (ETNT) using an infrared camera to detect and measure neglect symptoms pre- and postintervention. Results: The median was 14 out of 15 (93%) attended sessions, indicating that the adherence to the exergames training sessions was high. There were no adverse events and no drop-outs during the exergame intervention. The individual cognitive and spatial exploration skills slightly improved postintervention (P=.06 to P=.98) and continued improving at follow-up (P=.04 to P=.92) in 5 out of 7 (71%) patients. Calibration of the ETNT was rather error prone. The ETNT showed a trend for a slight median group improvement from 15 to 16 total located targets (+6%). Conclusions: The high adherence rate and absence of adverse events showed that these exergames were feasible and safe for the participants. The results of the amount of exergames use is promising for future applications and warrants further investigations—for example, in the home setting of patients to augment training frequency and intensity. The preliminary results indicate the potential of these exergames to cause improvements in cognitive and spatial exploration skills over the course of training for stroke patients with VSN symptoms. Thus, these exergames are proposed as a motivating training tool to complement http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 1 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al usual care. The ETNT showed to be a promising assessment for quantifying spatial exploration skills. However, further adaptations are needed, especially regarding calibration issues, before its use can be justified in a larger study sample. (JMIR Serious Games 2017;5(3):e17) doi: 10.2196/games.7923 KEYWORDS exergames; eye tracking; virtual reality; visuospatial neglect; feasibility By creating such a VR system, REWIRE aimed to facilitate its Introduction use for stroke patients discharged from the hospital to allow continuation of the rehabilitation process within their own Unilateral spatial neglect (USN) is characterized by the inability homes. A variety of home-based VR systems already exist for to detect, respond, or orient toward stimuli presented on the stroke patients mainly focusing on motor recovery [46-49], but contralateral side of a brain lesion . Being a neurological none exist for USN. Therefore, the consortium designed, among disorder of attention, USN can affect the auditory, visual, or others , exergames for the treatment of visuospatial neglect motor system [2-4]. With 43% in the acute phase and 17% at 3 (VSN) (VSN being a subtype of USN ) [41,51]. Exergame months poststroke, USN is the most common and persistent is a portmanteau of the words exercise and game , allowing problem associated with lesions of the right temporoparietal the patients to exercise their skills through gaming. In contrast cortex . Furthermore, USN patients share an unawareness of to games that are designed for diversion for healthy persons, their deficits to different extents. This anosognosia, combined exergames should follow therapeutic principles—for example, with an associated reduction in the ability to cope with activities the principles of exercise training, such as specificity and of daily living , typically results in longer rehabilitation progression , or adopting the training method of shaping periods [7-10]. Therefore, USN is a predictor of poor outcome , including frequent feedback and the selection of tasks in stroke patients and an added burden for the health care system addressing the individual deficits of patients. The REWIRE [7,8,11] requiring efficient treatment modalities [2,12-14]. consortium adopted the principles of exercise training as A variety of accepted and proven traditional methods exist to described by Hoffman  to design the neglect exergames. treat USN [2,15-19], such as pharmacological interventions Therefore, the games include the principles of (1) specificity, , different physiological sensory stimulations [21-23], and implying that the required performance of each game cognitive behavioral training . A combination of multiple corresponds to the goal of the game (to explore the neglected approaches to develop a personalized rehabilitation process is space) and (2) overload and progression, stating that the recommended [25,26] together with use of a battery of tests to components being used must be exercised at a level the patient assess USN rather than a single sole assessment [14,27]. is not normally accustomed to and the patient should progress However, none of these traditional methods could completely once accustomed to a level. In order to quantify training rehabilitate the condition, and rehabilitation methods progression from simple to complex within each game, the investigating new approaches are warranted. REWIRE consortium used Gentile’s taxonomy of motor skills as a template to develop the exergames (see Borghese et al  Virtual reality (VR), defined as “an advanced form of and Wüest et al  for more detail). Due to the nature of human-computer interface that allows the user to ‘interact’ with neglect and the related unawareness of neurological deficits , and become ‘immersed’ in a computer-generated environment it is important to test such a novel intervention with the target in a naturalistic fashion”  shows some preliminary evidence patient population in a surrounding where close monitoring is favoring its use, and further investigations in stroke possible and feasibility of the approach can be tested. Feasibility rehabilitation may complement traditional USN treatment may cover aspects such as adherence, safety, and attrition to methods [29-32]. VR methods provide a safe copy of the real the novel intervention or whether the intervention and environment while allowing the creation of customized assessments all run smoothly . rehabilitation programs through progressive, repetitive training with immediate feedback [13,19,26,33,34]. Promising VR Mainetti et al  and Sedda et al  already tested a former instruments exist both for the assessment [35-39] and version of the REWIRE VSN exergames in a single-case study rehabilitation [30-32,40-44] of neglect . The VR assessments design involving a neglect patient in the chronic stage. The were not only able to accurately detect USN patients but also results were promising in terms of a positive attitude of the made USN-related symptoms visible that were previously not patient toward the exergames and in showing a trend for identified with conventional assessments [26,33,34]. The VR improvement of the VSN-related deficits in daily life. Based systems tested for rehabilitation, however, were mostly complex on the experience with the exergames of this single user together to set up or used rather expensive tools (eg, head-mounted with feedback on their usability, the exergames were adapted displays or cyber gloves), restricting their use to laboratory and improved and then tested in this study for the first time in settings. a case series of patients. We aimed to test the exergames in early stroke patients shortly before their discharge to home. This time The European research consortium Rehabilitative Wayout in point was chosen to include as realistic a target population as Responsive Home Environments (REWIRE) developed a possible while still guaranteeing safety and supervision of the nonimmersive VR system for stroke patients using portable patients playing the exergames in the supportive environment devices with good performance and affordable equipment . of the rehabilitation clinic. Specific aims were to determine the http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 2 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al feasibility of the exergames with minimal supervision in terms brain injury other than stroke, if severe apraxia was of (1) implementation of the intervention, including adherence, present—measured as less than 5 points on the Apraxia Screen attrition, and safety, and (2) limited efficacy testing, aiming to of TULIA (test for upper limb apraxia) (AST) —or if other document possible effects on VSN symptoms in patients early noncontrolled medical conditions (eg, chronic pain, drug abuse) after stroke. were present. Patients with a left brain lesion due to a first stroke were excluded because the exergame difficulty levels were Methods designed to progress from the right (easy) to the left (difficult) side of the computer screen. An option to run the games Study Design vice-versa (from left to right) was not available. We adopted a quasi-experimental pretest-posttest design with All patients signed written informed consent before study entry. a subsequent follow-up to test the feasibility of the exergames Ethical approval for the study was received from the local ethics in a case series of stroke patients with VSN symptoms. As we committees (Zurich No. 2014-0543 and Bern No. 389/2014) as aimed to assess implementation of the exergames, thus testing well as from the Swiss agency for the authorisation and if our intervention can be fully implemented as planned and supervision of therapeutic products (Swissmedic, proposed, an uncontrolled pretest-posttest design is appropriate 2015-MD-0003). The latter approval was required as the . A broad variety of definitions exist for the concept of case software was not yet certified with the European Community series in literature . For our study, we used the definition marking for medical devices. The study is registered at of a case series as being a “report on a series of patients with ClinicalTrials.gov [NCT02353962]. an outcome of interest” . Recruiting a small convenience Setup sample was ideal for the planned limited efficacy testing, as we aimed to gain intermediate rather than final outcomes in this Patients were seated at a table in front of a 21-inch computer feasibility project, which allowed us to plan a shorter follow-up monitor at a distance of 60 to 65 cm in order to provide optimal period . eye tracking (Figure 1). We chose a seated position to allow more patients to participate (eg, wheelchair users) and avoid Patients exhaustion through standing in an upright position. A Identification of potential patients for this project was carried height-adjustable chin rest (Novavision GmbH) was mounted out by staff neuropsychologists and occupational therapists in on the table to avoid compensatory head movements while 2 collaborating rehabilitation clinics (Klinik Bethesda playing the exergames. Instead of a mouse to control games, a Neurorehabilitation, Parkinson-Zentrum, Epileptologie, haptic Falcon Novint device (Novint Technologies) was used. Tschugg, Bern, and Zürcher RehaZentrum Wald, This enabled individuals to experience a realistic sense of touch Faltigberg-Wald, Zurich). They screened all incoming stroke by providing simulated sensory feedback when reaching for patients with a diagnosis of VSN for eligibility in this study. and grasping virtual objects . The Falcon Novint device can We aimed for at least 5 participants, as this amount is considered be handled with one hand only, allowing stroke patients to play the minimum reasonable number of independent subjects in a the exergames with their nonaffected hand. The device was group to combine their data . Fewer than 5 patients are placed at the side of the computer monitor at a distance allowing usually presented in a descriptive, narrative form of individual ease of reach for the patients. The nonaffected upper extremity case reports. We strived for a maximum of 10 patients as was positioned in approximately 45° shoulder abduction, 70° recommended by Abu-Zidan et al . We included patients to 90° elbow flexion, and the forearm fully pronated. All with a right brain lesion (RBL) due to a first stroke 15 to 180 participants were expected to independently complete 15 training days after the cerebral event and a diagnosed VSN as measured sessions while being monitored by a supervising therapist. The by the Catherine Bergego Scale (CBS) . Inclusion criteria supervision included observation of the patient during the were being able to sit in a chair or wheelchair with a backrest intervention giving assistance where appropriate (eg, using the for 45 minutes, being at least 18 years old, and having a clear menu to start a new game). Observation was necessary for view (with or without vision aids) of a computer screen placed assistance if potential software difficulties occurred and for at a distance of 60 to 65 centimeters from patient’s face. VSN safety reasons for the patient, the latter being a regulation of patients were excluded if their neglect was diagnosed as due to the collaborating clinics. http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 3 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al Figure 1. Setup of the exergames training station. stimulus, the patient selected 3 to 4 REWIRE VSN exergames Exergames from the game menu to be played in each session. The choice The intervention program consisted of a series of 9 exergames was based on personal interest of the patient, which was assumed performed while seated. The games were designed to simulate to enhance motivation while playing. During the 3-week real-world tasks, such as cooking from a recipe, going for a intervention time, patients were allowed to change games if walk with a dog, or doing a puzzle (for detailed game they wanted to test another one or felt bored with the previously information on 4 games, see Pirovano et al ). The Falcon played game. After a break of 4 weeks, a follow-up measure Novint represented, for example, a dog leash by simulating a was performed aiming to test the training principle of pull from the dog to the left or right side of a virtual walking reversibility, which states that the ability to maintain path. The increase in difficulty of all games during the training performance is reduced when the training stimulus (the course was accomplished according to Gentile’s taxonomy of exergames) is removed. motor skills . Using this systematic classification to design Assessments the exergames allowed us to design a theory-based rehabilitation program that followed the principles of exercise training (see Primary Outcome Hoffman  and Ammann et al  for detailed descriptions In order to measure the likelihood and extent to which our of these principles). Playing time per game was adjusted from intervention can be fully implemented as planned and proposed 1 to 10 minutes per game depending on the patient’s ability to , we designed a training diary as a protocol to document concentrate playing the VR game while maintaining a seated attrition, adherence, and safety issues. This training diary was position. After initial training and instructions were given by on hand in the collaborating clinics and completed after each the research team, all subsequent game adjustments during the training session by the clinic staff in presence of the participating intervention were performed by clinic staff (occupational patient. The type of games played including difficulty level therapists and neuropsychologists) in accordance with the according to the Gentile’s taxonomy, effective training time, patient’s wishes. and patient subjective statements regarding their perceived Intervention Protocol health condition after training (posed question: “How do you feel after training: fit or tired?”) were all noted in the training The VR-based VSN training intervention took place in the 2 protocol. Additionally, any adverse events related to the collaborating rehabilitation clinics serving as an additional exergames intervention were noted. Potential adverse events therapy option to the standard program, which comprised daily could have been a recurrent stroke or other medical emergencies occupational, physical, and neuropsychological therapy. Each due to the early stage of recovery or an epileptic seizure or patient was asked to attend 5 30- to 45-minute sessions per week cybersickness due to playing the exergames . For attrition, for 3 weeks. The supervising therapist individually adjusted the the number of participants lost during the intervention was intensity of playing the exergames by changing the difficulty registered. For adherence, participant engagement with the level or game duration in the game menu and by deciding if intervention was noted. We expected a good adherence to the short breaks between each game would be necessary or not. In intervention, defined as an attendance of at least 50% of the accordance with the training principle of individuality , maximum 15 possible training sessions. Adherence was then which states that people respond differently to the same training http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 4 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al calculated as the number of completed training sessions as a Inventory (ZüMAX), and Neglect Test (NET) were administered percentage of the maximum 15 possible training sessions. by the research staff at baseline and after the intervention. After a 1-month follow-up, the ZüMAX and NET were repeated either Secondary Outcomes in one of the collaborating clinics or at the patient’s (new) residence (home or retirement home), depending on the length Overview of rehabilitation stay. In order to test limited efficacy of our intervention , the Eye Tracker Neglect Test (ETNT), Zürich Maxi Mental Status Figure 2. Setup of the Eye Tracker Neglect Test. screen with the midsagittal plane of the trunk aligned with the Spatial Exploration Skills center of the screen. An initial calibration of the Eye Tribe The ETNT is an adapted version of the cancellation test Tracker camera was then followed by 1 test trial with only 4 developed by Rabuffetti et al , aiming to assess symptoms targets and 8 distractors and the ETNT with 60 stimuli. A of neglect. In contrast to the original test, in which targets are stimulus was counted as being found (being circled) if the tagged by finger touch as measured by a touch screen, target patient maintained his or her point of gaze for at least 0.4 detection is operated by eye fixation as measured by an eye seconds within an area surrounding the stimulus with a diameter tracker (Figure 2). The ETNT display consists of a uniform of 7% of the total screen width, in keeping with Blignaut et al distribution of 60 stimuli including 20 targets (squares) and 40 . There was no time constraint; patients were instructed to distractors (other than square shapes) divided equally into 30 inform the researcher when they had finished the test. This stimuli (10 targets, 20 distractors) on the right and left sides of procedure was chosen to impose no stress on the patient while the computer screen. The eye point of gaze was tracked with exploring the targets on the screen. However, if the patient got the Eye Tribe Tracker camera (Eye Tribe). Eye tracking is the lost or became tired, the researcher present during the test asked process of using sensors to locate features of the eyes and the patient if he or she had the impression of having found all estimate where someone is looking . The technology relies targets and then stopped the test depending on the patient’s on infrared illumination so that it does not interfere with the response. visual scenario. Since the system tracks eye movements relative The Neglect Test (NET) consists of 7 paper-and-pencil subtests to the sensor/screen, it is necessary to fix the head position, (letter and star cancellation, copying 3 figures, and line crossing since head movements would be wrongly assumed as eye and bisection with a total possible score of 70 points) and 10 movements. Therefore, the patient’s head was fixed on a chin behavioral subtests (representational drawing, scanning 3 rest. In our study, each participant was seated in front of the pictures, menu and article reading, telling time, setting time on http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 5 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al a digital and analog watch, and address copying with a total Likert scale (ranging from 1=severe difficulties to 5=no possible score of 100 points) designed to identify a wide variety difficulties). The degree of unawareness for VSN was quantified of visual neglect behaviors . It has been shown to be a robust as proposed by Vossel et al  (see Figure 3). predictor of VSN and is a predictor of functionality after stroke This anosognosia index (AI) will be smaller than 0 if the patient . To assess the level of anosognosia for VSN after stroke, suffers from anosognosia, indicating an overestimated self-ratings of performance in 6 subtests of the NET (figure self-performance to what objectively has been performed. If the copying, star cancellation, line crossing and bisection, patient is able to rate his or her performance realistically, thus representational drawing, and article reading) were contrasted being below or matching the external rating, the index becomes with external performance ratings of the examiner on a 5-point equal to or greater than 0, indicating no signs of anosognosia. Figure 3. Formula for anosognosia index. differences in the NET and ZüMAX between all 3 measurement Cognitive Skills time points . We analyzed the data for each individual and The ZüMAX is a domain-specific assessment tool measuring for the whole group. The fact that the ZüMAX and NET cognitive impairment by evaluating executive function, comprise subtests and the NET additionally provides a language, praxia, visual perception and construction, and conversion table to transform raw scores into standard scores learning and memory (see Tobler-Ammann et al  for a allowed us to use the Wilcoxon signed rank test not only on a detailed description of the test). Each of the 5 domains allows group level but also on an individual level. For calculations per a maximum score of 6 points, with a maximum possible test patient, we used the achieved standard scores of each subtest score of 30 points, representing optimal cognitive functioning. as variables, resulting in 17 variables (corresponding to the 17 The ZüMAX has moderate to good test-retest reliability for the NET subtests) for the NET and 5 variables (corresponding to total test scores in patients 6 months or more poststroke and the 5 ZüMAX domains) for the ZüMAX. For the analysis on a may discriminate between this patient group and healthy age group level, we compared the achieved total scores per and gender matched persons . The ZüMAX visual perception measurement point of the 7 patients. and construction domain is the one indicating VSN symptoms. The ETNT data were provided by the software described in The task for visual perception is to recognize and name degraded Rabuffetti and colleagues . A subset of the relevant figures, unfamiliar scenes, and a face. The task for visual indexes—namely those that were related to visual construction consists of copying a figure. This assessment was perception—was used for data analysis as only these items were chosen due to its advantage of providing both general suitable for the adapted test version. As the ETNT software information about poststroke cognitive impairment and provided 1 value per index and patient, we used the Wilcoxon neglect-specific information and because of its origin in signed rank test to analyze post- to preintervention changes Switzerland where the study took place and, therefore, matching within the sample. Additionally, we graphically displayed the the cultural background of the participants. individual changes post-pre intervention by drawing the Data Analysis performed search path and fixation points and creating heat maps to visualize group changes post-pre intervention. Data analysis was carried out using SPSS for Windows version 23.0 (IBM Corp). A Shapiro-Wilk test was administered and In order to perform an a priori power analysis to determine the quantile-quantile plots were drawn to test normality of the data. minimum sample size for a future randomized controlled trial, The results confirmed our assumption of nonnormally distributed we calculated the effect sizes for the secondary outcome data due to the small sample size (P ≤.05 for most parameters). measures. We applied the Cohen formula for nonparametric We therefore used nonparametric tests for data analysis. tests  (see Figure 4). Accordingly, small, medium, and large Accordingly, a Wilcoxon signed rank test was adopted to effect sizes were labeled as r=0.1, 0.3, and 0.5, respectively compare post- with preintervention results and follow-up with . The level of significance was set at P ≤.05. postintervention results. The Friedman test was used to test for Figure 4. Cohen formula for nonparametric tests. http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 6 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al therefore taking part in the VR exergaming program including Results baseline, postintervention, and 3-month follow-up measures. Reasons preventing patients from participating were suffering Overview from a right-sided VSN due to a left brain lesion, having a severe From the 18 VSN patients consecutively screened for eligibility apraxia (fewer than 5 points on the TULIA (AST) screening in both clinics from March 2015 to March 2016, 7 patients instrument, and being in a poor health condition confining them (39%) were eligible and consented to participate in this study, to bed. Patient characteristics are presented in Table 1. Table 1. Patient characteristics. a b,i c,j Patient Age, years Sex Days post- Handedness/ Education Locomo- RBL CBS AST stroke at affected hand tion stroke type study entry (function) d e P1 64 M 25 ischemia R/L 7 12 PE WC (none) P2 74 M 29 ischemia R/L PE 17 12 (back) P3 64 M 114 ischemia R/L PE WC 5 12 (none) P4 70 M 32 ischemia R/L WC 6 12 SE (back) P5 53 M 42 ischemia R/L PE W 5 12 (none) P6 78 F 35 hemor- R/L SE W 10 12 rhage (back) P7 77 F 47 hemor- R/L PE WC 16 9 rhage (back) IQR 25 64 — 29 — — — — 5 12 50 70 — 35 — — — — 7 12 75 77 — 47 — — — — 16 12 RBL: right brain lesion. CBS: Catherine-Bergego Scale. AST: Apraxia Screen of TULIA. PE: primary education. WC: wheelchair. W: walker. SE: secondary education. IQR: interquartile range. Maximum score = 30 (severe neglect); 0 points = no neglect. Maximum score = 12 (no apraxia); threshold for apraxia: 9 points; severe apraxia: 5 points. 1 game per training session. The supervising therapists adapted Primary Outcome and individually progressed the patient training protocols on a An overview of individual (P1-P7) and group (interquartile weekly basis during the exergames intervention in accordance range [IQR], mean) results in the training protocol is shown in with patient progress. If, for example, the patient got bored with Multimedia Appendix 1. There were no adverse events and the current difficulty level of the played game or the therapist drop-outs during the intervention. A median attendance of 14 observed that the game was played without effort, the therapist (IQR 12-15) training sessions (maximum 15 sessions) was modified the difficulty level within each game. However, if the achieved, which corresponds to a median adherence of 93% patient had reached the most difficult level, the therapist (IQR 80%-100%). Reasons for nonparticipation were of replaced easy games with more complex ones (ie, games organizational or medical nature (eg, overlap with other therapy including more distractors or moving objects). An analysis of sessions or due to fatigue) rather than because of motivational the progress as measured by the achieved game scores was factors. All patients played 2 to 4 games and repeated at least therefore not feasible, as progression in difficulty resulted in a http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 7 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al temporary decrease in game scores. Instead, the progress in the camera (see Multimedia Appendices 3 and 4 for all graphs of exergames training of the 7 individual patients was documented individual post-pre ETNT search paths and fixation points). weekly according to the Gentile’s taxonomy of motor skills. Figure 6 shows the heat maps of the pre- and postintervention These results are shown in Multimedia Appendix 1. and differences in post-pre detected targets of the ETNT. An overview of ZüMAX, NET, and AI scores and group changes Secondary Outcomes pre-, postintervention, and at follow-up is summarized in Multimedia Appendix 5 and graphically displayed in Figure 7 Spatial Exploration and Cognitive Skills (overview) and Multimedia Appendix 6 (individual results per An overview of the individual ETNT scores and group changes outcome measurement). The individual changes in the ZüMAX post- to preintervention is shown in Multimedia Appendix 2. and NET assessments are presented in Multimedia Appendix Figure 5 shows 2 examples of pre-post intervention search path strategies and fixation points as measured by the eye tracker Figure 5. Examples of pre- and postintervention results of the Eye Tracker Neglect Test search paths and fixation points of P3 and P4. http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 8 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al Figure 6. Heat maps of the preintervention, postintervention, and difference post-pre results of the Eye Tracker Neglect Test. Figure 7. Graphical overview of preintervention, postintervention, and follow-up Zürich Maxi Mental Status Inventory, Neglect Test, and anosognosia index results. Appendix 2). The postintervention performance showed a Eye Tracker Neglect Test median decline of 2 (IQR 0-4) missed targets on the left side of the screen and a median increase of 1 (IQR 0-3) missed target Group Level on the right side of the screen. The heat maps (Figure 6) indicate The pre-post assessment showed a median group trend of slight that the ability to detect targets in the upper left portion of the improvement in the total located targets from 15 to 16 (+6%) computer screen increased postintervention and remained pre-post, which was concomitant with an increasing median substantially unmodified otherwise. The results further showed total test duration (+33.9 seconds pre-post) (Multimedia http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 9 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al an unchanged median group trend pre-post intervention Individual Level regarding the neglect score, the median latency, and proximity. On an individual level, P1, 2, 5, and 6 improved from pre- to There were no statistically significant changes pre-post postintervention in the ZüMAX total scores, while P3 and 4 intervention for any ETNT parameters (Multimedia Appendix declined and P7 remained unchanged (Multimedia Appendix 2). 6). The post–follow-up scores declined in P1 and P7, while P2 to P6 still improved their post–follow-up scores, with P3 and Individual Level P4 declining pre-post intervention. In the ZüMAX visual P4 improved from 5 to 15 total located targets pre-post perception subtask (recognizing and naming degraded figures), intervention (Multimedia Appendix 2 and Figure 5). The only 3 of the 7 patients stayed unchanged from pre-post to follow-up individual worsening pre-post regarding the left spatial (P3, P5, P6), while the largest progression was apparent in P7, exploration skill was P3, with no target missed preintervention with a clear decline of 3 points after termination of the and 4 targets missed postintervention (Figure 5). Most exergames intervention (Multimedia Appendix 6). In the second participants (6/7, 86%) started their search in the right sector ZüMAX subtask related to neglect (visual construction: figure and scanned leftwards vertically (Multimedia Appendices 3 and copying), 3 patients performed the pre- and postintervention 4), while P3 started in the upper left sector and scanned assessments with unchanged scores (P3, P6, P7), and 3 patients top-down horizontally (Figure 5). Additionally, 4 out of 7 (57%) showed a slight decline post–follow-up (P1, P3, P5). started their search on the right side of the screen, 2 out of 7 (29%) were able to change the starting point from right to left, Discussion and 1 participant (P3) started the search on the left side of the screen pre- and postintervention (Multimedia Appendices 3 and Principal Findings 4). This study evaluated the feasibility of an exergames intervention Neglect Test aimed to affect VSN symptoms in patients early poststroke in terms of implementation (adherence, attrition, and safety) and Group Level limited efficacy testing by documenting changes in VSN The NET showed statistically significant improvements pre- to symptoms. The exergames intervention was tolerated well by postintervention (P=.01 to P=.03) in the total score and both all participants and was mainly performed without major subtests as well as in the Friedman test (P=.01 to P=.02) difficulties, showing that its implementation in the clinical (Multimedia Appendix 5). The AI results showed a group trend setting was feasible. With 0 out of 7 (0%) attrition, no adverse toward zero (median 0.08 pre, 0.04 post, 0 follow-up), indicating events, and a median adherence rate of 14 out of 15 sessions a trend toward perfect awareness of oneself (Multimedia (93%), the compliance of the patients to the exergames was Appendix 5). excellent. Such a result was possibly due to the clinic staff’s commitment, as the VR intervention was smoothly integrated Individual Level into the daily therapy schedule of the clinic. However, as we P1 and P2 declined at follow-up in the NET total scores, while aimed to test the fit of our intervention in a real-world setting, P3 to P7 showed further improvement. P1, P5, and P7 we prioritized clinic constraints over optimal conditions and significantly changed in their NET total scores, P1 settings. As a consequence, this priority reduced potential post–follow-up (P=.04) and P5 and P7 pre-post–follow-up omissions of training sessions as described in purely home-based (Friedman test; P=.01 and P<.001, respectively) (Multimedia VR interventions . There, the level of use of the VR system Appendix 7). The post–follow-up result of P1 also showed a was variable and fell far short of recommendations, despite the large effect (r=–.80), indicating a large decline in the NET weekly or biweekly visits of a researcher to the patients’ homes scores postintervention, especially in the paper-and-pencil to check progress and retrieve data. subtasks (Multimedia Appendix 6). Analyzing NET scores by subtests, all patients improved pre- and postintervention in the Other studies testing novel VR systems for upper limb stroke paper-and-pencil subtests (Figure 7), while in the behavioral rehabilitation have also shown high levels of adherence to the subtests, all patients improved pre- to postintervention except training intervention [74-76]. However, these patients were in for P3 who remained unchanged (Multimedia Appendix 6). the chronic stage of recovery and did not suffer from USN. The Two patients (P3 and P7) suffered from anosognosia with a single participant with USN of the Duckneglect study (Mainetti trend of aggravation from pre- to follow-up assessments (Figure et al ), who also was in the chronic stage of stroke recovery, 7). P1, P2, and P4 showed no signs of anosognosia at follow-up showed an excellent adherence to the exergames, in keeping (AI index=0), while P5 and P6 showed a trend toward an with our case series. increasing AI index, underestimating their actual performance Regarding the exergames training, the median duration per (Multimedia Appendix 6). session was 30 (IQR 23-30) minutes, which fell short of the Zürich Maxi Mental Status Inventory planned 30 to 45 minutes of training time. For our study, we decided to set a timeframe rather than an exact exposure time, Group Level because little is known about the optimum duration and The ZüMAX showed improvements in the total scores from patterning of training exposure to virtual environments . pre- to postintervention to follow-up (Figure 7) that were not Possible reasons for the rather short training sessions in our statistically significant (P=.29 to P=.45, median +2 points sample were twofold: either patients (eg, P2 and P3) were quite pre-post, +1 point post–follow-up) (Multimedia Appendix 5). fit and finished the planned exergames session early or, http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 10 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al conversely, were too tired to play longer (eg, P1). In our sample, some of the improvements. A further possible reason is 5 out of 7 (71%) patients indicated being fit after most trainings spontaneous recovery of VSN symptoms not only during the (median 13 out of 15 [87%] possible sessions), excluding fatigue acute phase after stroke but also during the following few weeks. as being a main reason for the rather short training time. P7, Paolucci et al , for example, reported a decrease of VSN however, being the only participant with a highly distinctive symptoms to 20% from 45% after 1 month poststroke, which VSN as measured with the NET, needed on average 34 minutes may also have occurred in our sample. Additionally, the to accomplish the games. These results highlight the importance heterogeneity in our sample regarding neglect severity—4 out of adjustability of the difficulty level of the exergames to the of 7 (57%) were only mildly affected with CBS scores between functional ability of the stroke patient , thus avoiding a 5 to 7 points (Table 1), while 2 out of 7 (29%) were severely decline in enjoyment level while playing . Given the affected (16-17 scores on the CBS)—might have influenced the uncertainty about optimal exposure together with our small and rate of improvements, too. However, our sample did not show highly varied sample (Table 1, CBS scores), future trials should a ceiling effect—being present if 15% or more participants focus on investigating optimal thresholds of exposure time achieve the highest possible score —as no participant corresponding to the degree of VSN severity. achieved the highest score in any of the outcome measurements. Furthermore, most patients continued improving their scores in The fact that there were no adverse events during the training the NET and ZüMAX assessments postintervention, achieving period in our case series was encouraging. Besides being lucky the highest scores after a break of 4 weeks (follow-up). Only that no recurrent stroke or other medical emergency happened P1 in both tests and P2 (NET) and P7 (ZüMAX) showed a during the intervention, the design of the games might have decline in scores from post to follow-up, which would contributed as well to the safety of our participants. For example, correspond to the training principle of reversibility [53,63] that implementing both stationary and in-motion conditions of the states that once a training stimulus is removed, performance virtual scenario together with the option of choosing between levels will eventually return to or below baseline. Comparing intertrial variability and no intertrial variability while gaming our efficacy testing results with literature was difficult, as studies allowed the patient to choose the optimal virtual environment with a similar setup, time point of measurement, and target to be challenged on the one hand but not be overwhelmed on group are scarce. There is evidence that training with VR the other hand (see Multimedia Appendix 1). Allocating these methods improve spatial attention and show transfer of improved options in difficulty level might have contributed to reducing spatial attention in activities of daily living in chronic neglect the risk of cybersickness while playing despite the stationary [30,32]. Kim et al  showed additional benefit for treating condition of the patient . When designing the setup of our cognitive impairment in stroke patients without VSN in the study, we intentionally planned a seated position to play the subacute phase of recovery when adding VR training to classical games. This allowed patients to fully concentrate on the cognitive rehabilitation. The evidence supports our findings exploration of the neglected space without having to invest that using VR systems to treat cognition in stroke patients is energy standing in an upright position. Furthermore, playing promising and feasible; however, further research is warranted the games in a seated position contributed to the prevention of and necessary to test its use in patients with VSN symptoms falls. Prahm et al , for example, also designed a game-based early poststroke. Future studies with a focus on treatment effects intervention in a seated position reporting no adverse events. using controlled research designs should be used to assess causal However, their participants were able-bodied adults. Wiloth et relationships between the game-based interventions and al  reported no adverse events in their game-based important patient outcomes. assessment to measure motor-cognitive function in people with dementia while they were standing on a movable platform. The median AI values in our sample ranged from 0.08 Although falls are highly prevalent in people with cognitive preintervention to 0.0 at follow-up. Comparing those results to impairment such as dementia , people poststroke bigger RBL stroke samples with USN—mean (SD) lower AI additionally suffer from motor impairment. Despite their –0.28 (0.5) for n=34 and mean (SD) higher AI –0.47 (0.5) for hemiparesis, our participants were all able to perform the games n=22; Vossel et al  and mean (SD) AI –0.16 (0.38) for n=55; and handle the Falcon Novint with the nonaffected hand. The Vossel et al —our 7 patients showed quite a high level of clinic staff reported that sometimes the more concentrated self-awareness for their visuospatial deficits, including P3 and or—toward the end of the training session—the more tired the P7 who scored below zero (indicating anosognosia) during all participants became while playing the exergames, the more they 3 measurements. Of the 7 patients, 3 continued increasing their tilted to the left side with their upper body. As this is a level of self-awareness postintervention to zero (P1, P2, P4), well-known phenomenon in VSN patients poststroke , we suggesting positive effects of time poststroke on anosognosia think our approach of offering gameplay in a seated position rather than our training intervention. However, time poststroke guaranteed patient safety. The rather tilted position, however, might not be a viable indicator for those continued did not prevent the participants from continuing to play the improvements in self-awareness of neglect, as Vossel and exergames. colleagues  found no differences in their AI values across their 3 patient subgroups differing in time since stroke onset. Our limited efficacy testing showed a group trend of Therefore, continued rehabilitation might be a plausible reason improvements in cognitive and spatial exploration skills. for those further improvements. However, looking at the other However, these changes cannot be exclusively attributed to the 4 patients, AI values showed a tendency toward worsening from exergames intervention. One reason is the ongoing VSN preintervention to follow-up, with P3 and P7 overestimating treatment in the rehabilitation clinic that might also explain and P5 and P6 underestimating their NET performance, although http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 11 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al they also had continued rehabilitation. There is evidence that P3 was able to detect preintervention, were due to calibration anosognosia for spatial deficits is not predominant, with different difficulties, as P3 was able to point at those 4 targets with his tasks evoking different degrees of awareness about the neglect hand. P1 and P6 were the only patients able to shift their search symptoms . As the AI is calculated on the basis of 4 starting points from the right to the left side from pre- to paper-and-pencil and 2 behavioral tasks of the NET, it might postintervention, indicating improvements in exploring the be that this mix of tasks also influenced the miscellaneous AI neglected side . Not surprisingly, the increased total test results. For example, Ronchi et al  found that anosognosia duration pre- to postintervention in our sample went along with level improved after performance of complex visuomotor (eg, slightly more detected targets. When the participant increases cancellation and drawing) and reading tests. By contrast, the the number of detected targets, it can be the case that previously self-rating in line bisection tasks was not related to actual task neglected targets are now detected albeit with a fairly large performance . Furthermore, as the AI test is designed to be latency. We interpret this as positive since more visual space performed after task execution, it might be that the patients were is actively explored but latency and concomitantly the total test able to correct their erroneous self-rating to some extent at least duration may therefore also increase. A future study including in the complex visuomotor tasks. Last but not least, the a larger sample and a control condition is, however, warranted repetition of the NET test over a relatively short time span might to substantiate or refute these findings. have influenced the AI results, too, as the patients knew that a We performed an a priori power analysis to determine the self-rating would follow after certain tasks. minimum sample size for such a future trial . Specifically, The ETNT results are to be considered preliminary and should we assessed the requirements for a randomized controlled study be interpreted with caution. Calibration difficulties with the Eye with an experimental group (receiving exergame-based therapy Tribe Tracker system (eg, most patients only reached 3 out of and usual stroke rehabilitation) and a control group (receiving 5 points in calibration quality scores) may have influenced the usual stroke rehabilitation only). Assuming an effect size of reliability of the setup and the accuracy of the results. The r=0.9 (based on our observed value for NET total scores, calibration consisted of eye-tracking a circle that moved around Multimedia Appendix 5), acceptable type I and II error the whole display. The difficulties experienced by patients in probabilities (0.05 and 0.20, respectively) may be obtained with following the rapidly moving circle and the requirement to look a minimum sample of 34 subjects per group for a 2-group at calibration points at the very left of the computer screen were pre-post-test design. To account for attrition, initial sample size the main reasons for the rather poor calibration results. Such should be increased to 45 subjects per group . Given the difficulties may produce visible effects (in Figure 5, for example, fact that only 18 potential participants were available within 12 P4 evidences a dense cloud of gaze points on the bottom right months of recruitment, we recommend collaborating with more corner during the postintervention assessment, where P4 than 2 clinics for such a trial. unsuccessfully tried to tag the 3 targets he could point at with Limitations and Future Work his hand). Baheux et al  also reported calibration problems The length of the training phase was rather short (ie, 3 weeks). with their 3-D haptic VR system coupled with an eye-tracking We deliberately did not choose a longer training period, as we device. They assumed that the VSN patient spectacle wear or primarily wanted to test the exergames’ feasibility and not their eye color might have been reasons for calibration difficulties. effect on VSN symptoms. On the other hand, the rather short However, these calibration difficulties notwithstanding, our training phase allowed us to keep the drop-out risk relatively ETNT results showed trends toward slight improvements in low (eg, due to discharge home during the training phase). In both total located and missed targets on the left side of the a next step, it would be important to test the exergame system’s screen. The heat maps display the increased ability to detect feasibility in patient homes to evaluate adherence, safety, and targets in the upper left portion of the computer screen attrition to using the system in this setting, as the provision of postintervention but remained substantially unmodified novel home-based rehabilitation options was the main goal of otherwise. However, the preintervention performance was REWIRE. In this setting, a longer training phase could be tested. already fairly good in our sample. Furthermore, the heat maps Furthermore, a progression as measured by the game scores show that the ETNT can identify neglected areas. This is in line should be implemented together with an immediate graphical with the Rehabilitation Gaming System by Maier et al  feedback after each training session to enhance motivation for using the Kinect motion capture system being equally able to playing the exergames. For this implementation, ideas from the measure symptoms of neglect. In contrast to our test, the stroke rehabilitation method of shaping , where frequent feedback patients in the chronic stage of recovery explored the neglected and encouragement during training are central, could be adopted. side with the paretic arm. In order to maximize confidence that changes in outcomes can The individual search strategy (Multimedia Appendices 3 and be attributed causally to the exergames intervention, a control 4) of most patients was comparable with those described by group in a pilot randomized controlled trial design would be Müri et al  and Rabuffetti et al , namely to start in the needed. The neglect exergames should further be designed to (extreme) right sector and scan leftwards vertically. This switch levels of difficulty (ie, progressing from the right to the contrasts with the search strategy demonstrated by the control left side of the screen or vice-versa). Designing this option subjects in these studies, which started in the upper left sector would allow recruiting stroke patients with a left-sided brain and scanned top-down horizontally (like reading). Only P3 lesion and VSN symptoms, too. By excluding them in our showed a nonneglect-specific search strategy (Figure 5). The 4 project we were aware that we would probably miss some missed targets in the left lower corner postintervention, which patients having ipsilesional neglect , which would have http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 12 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al made a participation in the exergames intervention feasible. in order to validate the derived ETNT measures of recovery However, as left-sided neglect is quite rare compared to after VSN. right-sided neglect , the risk of missing such an ipsilesional Conclusion neglect patient was relatively low. This study showed that patients adhered well to the REWIRE The ETNT could further be developed regarding the following: neglect exergames intervention with no drop-outs, no adverse events, and an adherence rate of 14 out of 15 sessions (93%). • Calibration procedure of the Eye Tribe Tracker by reducing We therefore judged this intervention to be safe and feasible the speed of the circle to be followed, for example for VSN patients early poststroke and appropriate for further • Software indexes, which were initially designed for the testing. Cognitive and spatial exploration skills, as evaluated touchscreen (hand-eye coordination) test. Indexes important using ETNT, NET (spatial exploration), and ZüMAX (cognition) for eye-tracking would be, for example, the cumulative assessments, improved in most patients from pre- to fixation duration, spatial distribution of fixations in the postintervention. The results of the amount of exergames use horizontal and vertical plane, or the number and amplitude is promising for future applications and warrants further of exploratory saccades as explored by Müri et al  investigations, for example, in the home setting of patients as • Collection of the search strategy patterns of age-matched a motivating training tool to complement usual care and support controls augmenting training frequency and intensity in RBL stroke Additionally, future work could correlate ETNT measures to patients with VSN. scores in standardized clinical scales, such as the NET scores, Acknowledgments BCT-A designed the study; provided support in designing the exergames; conducted the acquisition, analysis, and interpretation of the data; and wrote the manuscript. EF and MR developed the software and exergames and contributed to the analysis and interpretation of data and writing of the manuscript. LW helped recruit the patients and edited the manuscript. EDdB, NAB, and RHK initiated the study and contributed to design, writing, and editing of the manuscript. All authors read and approved the final manuscript. This work was partially supported by the REWIRE project (www.rewire-project.eu) and funded by the European Commission under the FP7 framework with contract 287713 and the Occupational Therapy Association of Switzerland. Author MR was supported by funding (Ricerca Corrente) from the Italian Ministry of Health. Many thanks go to the collaborating clinics who made the patients recruitment possible, namely to Klaus Meyer, MD, Klinik Bethesda, Tschugg, Canton of Berne, Switzerland, and his team of neuropsychologists and to Andreas Sturzenegger, MD, Klinik Wald, Wald, Canton of Zurich, Switzerland, and his team of occupational therapists. Laura Wiederkehr, former master student of the ETH Zurich, is very much appreciated for her scientific and administrative support and for performing the measurements. Further thanks goes to Gabriel Baud Bovy (Istituto Italiano di Tecnologia, Genova) for his work on the Novint Falcon haptic device. Finally, many thanks to Martin J Watson, PhD, for proofreading the manuscript for English and structure. Conflicts of Interest None declared. Multimedia Appendix 1 Overview of individual and group results in the training protocol. [PDF File (Adobe PDF File), 33KB-Multimedia Appendix 1] Multimedia Appendix 2 Overview of individual Eye Tracker Neglect Test scores and group changes pre- to postintervention. [PDF File (Adobe PDF File), 45KB-Multimedia Appendix 2] Multimedia Appendix 3 Pre- and postintervention results of individual Eye Tracker Neglect Test search paths. [PNG File, 432KB-Multimedia Appendix 3] Multimedia Appendix 4 Pre- and postintervention results of individual Eye Tracker Neglect Test fixation points. http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 13 (page number not for citation purposes) XSL FO RenderX JMIR SERIOUS GAMES Tobler-Ammann et al [PNG File, 710KB-Multimedia Appendix 4] Multimedia Appendix 5 Overview of Zürich Maxi Mental Status Inventory, Neglect Test, and anosognosia index scores and group changes preintervention, postintervention, and follow-up. [PDF File (Adobe PDF File), 40KB-Multimedia Appendix 5] Multimedia Appendix 6 Graphical display of individual Zürich Maxi Mental Status Inventory, Neglect Test, and anosognosia index scores. [PNG File, 324KB-Multimedia Appendix 6] Multimedia Appendix 7 Individual changes in the Zürich Maxi Mental Status Inventory and Neglect Test assessments. [PDF File (Adobe PDF File), 42KB-Multimedia Appendix 7] References 1. 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J Neurol Neurosurg Psychiatry 1999 Jul;67(1):35-38 [FREE Full text] [Medline: 10369819] Abbreviations AI: anosognosia index AST: Apraxia Screen of TULIA CBS: Catherine Bergego Scale ETNT: Eye Tracker Neglect Test IQR: interquartile range NET: Neglect Test RBL: right brain lesion REWIRE: Rehabilitative Wayout in Responsive Home Environments TULIA: test of upper limb apraxia USN: unilateral spatial neglect VR: virtual reality VSN: visuospatial neglect ZüMAX: Zürich Maxi Mental Status Inventory Edited by G Eysenbach; submitted 26.04.17; peer-reviewed by P Standen, B Ballester, N Skjaeret; comments to author 31.05.17; revised version received 13.07.17; accepted 31.07.17; published 25.08.17 Please cite as: Tobler-Ammann BC, Surer E, de Bruin ED, Rabuffetti M, Borghese NA, Mainetti R, Pirovano M, Wittwer L, Knols RH JMIR Serious Games 2017;5(3):e17 URL: http://games.jmir.org/2017/3/e17/ doi: 10.2196/games.7923 PMID: 28842388 ©Bernadette C Tobler-Ammann, Elif Surer, Eling D de Bruin, Marco Rabuffetti, N Alberto Borghese, Renato Mainetti, Michele Pirovano, Lia Wittwer, Ruud H Knols. Originally published in JMIR Serious Games (http://games.jmir.org), 25.08.2017. This is an open-access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work, first published in JMIR Serious Games, is properly cited. The complete bibliographic information, a link to the original publication on http://games.jmir.org, as well as this copyright and license information must be included. http://games.jmir.org/2017/3/e17/ JMIR Serious Games 2017 | vol. 5 | iss. 3 | e17 | p. 18 (page number not for citation purposes) XSL FO RenderX
JMIR Serious Games – JMIR Publications
Published: Aug 25, 2017
Keywords: exergames; eye tracking; virtual reality; visuospatial neglect; feasibility
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