Authors: Jisun Yoon, MD Min Ho Chun, MD, PhD Sook Joung Lee, MD Bo Ryun Kim, MD
Brain Tumor
Affiliations: From the Department of Rehabilitation Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul (JY, MHC); Department of Physical Medicine and Rehabilitation, Dong-A University College of Medicine, Busan (SJL); and Department of Rehabilitation Medicine, Jeju National University Hospital, University of Jeju College of Medicine, Jeju, Republic of Korea (BRK).
ORIGINAL RESEARCH ARTICLE
Effect of Virtual RealityYBased Rehabilitation on Upper-Extremity Function in Patients with Brain Tumor Controlled Trial
Correspondence: All correspondence and requests for reprints should be addressed to: Min Ho Chun, MD, PhD, Department of Rehabilitation Medicine, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-Ro 43-Gil, Songpa-gu, Seoul 138Y736, Republic of Korea.
ABSTRACT Yoon J, Chun MH, Lee SJ, Kim BR: Effect of virtual realityYbased rehabilitation on upper-extremity function in patients with brain tumor: controlled trial. Am J Phys Med Rehabil 2015;94:449Y459.
Objective: The aim of this study was to evaluate the benefit of virtual realityYbased rehabilitation on upper-extremity function in patients with brain tumor.
Disclosures:
Design: Patients with upper-extremity dysfunction were divided into age-
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
matched and tumor typeYmatched two groups. The intervention group performed the virtual reality program 30 mins per session for 9 sessions and conventional occupational therapy 30 mins per session for 6 sessions for 3 wks, whereas the control group received conventional occupational therapy alone 30 mins per session for 15 sessions for 3 wks. The Box and Block test, the Manual Function test, and the Fugl-Meyer scale were used to evaluate upper-extremity function. The Korean version of the Modified Barthel Index was used to assess activities of daily living.
Results: Forty patients completed the study (20 for each group). Each group 0894-9115/15/9406-0449 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/PHM.0000000000000192
exhibited significant posttreatment improvements in the Box and Block test, Manual Function test, Fugl-Meyer scale, and Korean version of the Modified Barthel Index scores. The Box and Block test, the Fugl-Meyer scale, and the Manual Function test showed greater improvements in shoulder/elbow/forearm function in the intervention group and hand function in the control group.
Conclusions: Virtual realityYbased rehabilitation combined with conventional occupational therapy may be more effective than conventional occupational therapy, especially for proximal upper-extremity function in patients with brain tumor. Further studies considering hand function, such as use of virtual reality programs that targeting hand use, are required. Key Words:
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Brain Tumor, Upper-Extremity Function, Virtual Reality, Occupational Therapy
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P
rimary brain tumors account for less than 2% of all malignancies and generally leave the affected patient with significant functional impairment.1,2 Aggressive treatments based on surgery, radiation, and chemotherapy frequently lead to improved survival rates for patients with brain tumors. Nonetheless, brain tumors continue to cause pronounced neurologic deficits despite these interventions. Cognitive impairment is the most commonly reported deficit, at an occurrence rate of 80%, followed by motor weakness (78%), visual-perceptual deficits (53%), sensory loss (38%), and bowel and/or bladder dysfunction (37%). The neurologic impairments are similar to those found in patients who have had a stroke or a traumatic brain injury.3 Rehabilitation therapy in patients with brain tumor has gained prominence during the past three decades, and several studies indicated that individuals with brain tumors make significant functional strides after rehabilitation.4Y7 For example, Huang et al.8 demonstrated that patients with brain tumor in acute inpatient rehabilitation centers had a decreased length of stay compared with patients with stroke and also achieved functional gains comparable with those of stroke survivors. Along the same lines, O’Dell et al.2 found that brain tumor patients with appropriate rehabilitative treatment achieved functional gains approaching those of patients with brain injury. Virtual reality (VR) can be defined as the Buse of interactive simulations created with computer hardware and software to present users with opportunities to engage in environments that appear and feel similar to real-world objects and events.[9 VR programs are used in various kinds of vocational training, including flight simulations for pilots and driving simulations for automobile operators.10 Recently, VR programs have also been incorporated into neurologic rehabilitation agenda to improve upper-extremity (UE) function,11 lower extremity function,12 and gait.12 In addition, VR is widely used in the field of brain disease for cognitive rehabilitation.13 Heretofore, most investigations of VR therapy have been directed toward improving motor function in patients with stroke and traumatic brain injuries. Several randomized controlled trials have compared VR-mediated therapy with conventional occupational therapy (OT) for the enhancement of UE function and have shown significant improvements in the Box and Block test (BBT) of manual dexterity, the Fugl-Meyer scale (FMS), the Manual Function test (MFT), and the Wolf Motor Function test score of UE motor ability.14,15
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To the best of the authors’ knowledge, no investigations have been performed to date regarding the effect of VR-based rehabilitation on the restoration of UE function in patients with brain tumor. The aim of this study was to evaluate the ability of VR-based rehabilitation to improve hand, arm, and shoulder function in these individuals. The primary outcome of this study was an improvement in UE function evaluated by the BBT, the MFT, and the FMS. The secondary outcome was an improvement in activities of daily living evaluated by the Korean version of the Modified Barthel Index (K-MBI). The authors hypothesized that combining VR-based rehabilitation with conventional OT would help to improve UE function in patients with brain tumor compared with conventional OT.
METHODS Study Participants Patients with UE dysfunction as a consequence of brain tumor were recruited from an inpatient clinic in the Department of Rehabilitation Medicine of the Asan Medical Center, Seoul, Republic of Korea, from March 1, 2011, through March 1, 2012. Inclusion criteria were as follows: (1) a brain tumor diagnosis with a stable status after the completion of proper management (surgery, chemotherapy, or radiation therapy); (2) patients with a Korean version Mini-Mental State Examination score of greater than 20 who are capable of understanding the therapist’s instructions; (3) a Brunnstrom stage of higher than 2 (2: hyperreflexia, emergence of spasticity and synergies, minimal voluntary movement in the affected limbs) corresponding to the affected UE; (4) a score on the Modified Ashworth spasticity scale of less than 2 (2: more marked increase in muscle tone through most of the range of motion but affected part is easily moved); and (5) motor power grade of the affected shoulder of higher than Bpoor[ (poor strength corresponds to inability to perform movements against gravity but complete range of motion when the pull of gravity is eliminated). Exclusion criteria were as follows: (1) a diagnosis of global aphasia; (2) decreased sitting balance; (3) a recurrent brain tumor; (4) perceptualcognitive dysfunction (visuospatial neglect and cognitive function evaluated by the Albert test16 and the Korean version Mini-Mental State Examination17); (5) musculoskeletal problems and/or peripheral neuropathy of the affected limb; and (6) medical instability (acute inflammation or infection such as pneumonia, urinary tract infection, and sepsis).
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The patients were allocated into two groups by developing the stratified random sampling numbers by dividing strata using two variables (age, type of tumor). All participants provided written informed consent before the initiation of the study. The study protocol was approved by the Research Ethics Committee of the Asan Medical Center.
Study Protocol The individuals in the intervention group carried out the VR programs described below for 3 wks at a frequency of 30 mins per day, three times per week (nine sessions). The patients in the intervention group also received conventional OT for 3 wks at a frequency of 30 mins per day, two times per week (6 sessions), whereas the control group received conventional OT alone for 3 wks at a frequency of 30 mins per day, five times per week (15 sessions). For the duration of this study, all participants received conventional rehabilitation including physical, occupational, and cognitive therapies of the same intensity and duration. Conventional OT consisted of range of motion exercises, fine motor training, and strengthening UE exercises.18 Range of motion exercises consisted of overhead pulley, range of motion arc, and inserting rings to a horizontal bar. Fine motor training consisted of turning coins, tapping of the thumb and the index finger, as well as inserting a piece of wood into small holes in a pegboard.19 Strengthening exercises consisted of upper body exerciser, sanding, weight pulley exercises, and using a Theraband or lifting a dumbbell. Each exercise took approximately 10 mins. VR-based rehabilitation was performed by an occupational therapist proficient in the use of the Interactive Rehabilitation and Exercise (IREX) Sys-
tem (Vivid Group, Toronto, Canada), described below (GestureTek Health, IREX). Therapists were blinded to the study design. The IREX System VR environment entails a television monitor, a video camera, a computer recognition glove, virtual objects, and a number of VR programs (Fig. 1). Video cameras placed the patients within the VR environment by analyzing their positions and movements. Computer recognition gloves also read the patients’ reactions (responsive movements) and transferred them to the VR system. The patient was able to see his/her own body movement in real time, which allowed the patient to be immersed inside the virtual environment. Six VR programs (Birds and Balls, Conveyor, Drums, Juggler, Coconuts, and Soccer) were selected from a total of 20 available programs (Fig. 2). The Birds and Balls program involves balls appearing on the screen from various directions. The balls burst into birds when the patient touches them by using his/her hand movements. The Coconuts program denotes a basket that moves from the left or the right across the screen in response to the patient’s arm movements. The aim of the game is to use the basket to catch the coconuts falling from the upper portion of the screen. The Conveyor program depicts two conveyor belts located at the left and the right hand side of the screen, with boxes appearing from either side. Patients are asked to use their hand movements to shift the boxes from one conveyer belt to the other. The Juggler program requires the patient to keep several balls simultaneously moving in the air with his/her hands. The Drum program asks the patient to use his/her hands to play a drum along with the rhythm of music. Finally, the Soccer program depicts a soccer ball flying toward the patient, who is asked to stop the ball by using his/her hand as a goalkeeper. These
FIGURE 1 The virtual reality experimental setup of the IREX System (Vivid Group, Toronto, Canada). www.ajpmr.com
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FIGURE 2 Six VR programs used in this study. A, birds and balls; B, conveyor; C, drums; D, juggler; E, coconuts; F, soccer.
six programs specifically demand UE movements such as shoulder flexor/adductor/abductor, elbow flexor, or elbow extensor muscles and can be performed in a standing position or a sitting position. Each program provided background music related to the game. Degrees of difficulty were set by the therapist or by the request of the patient, ranging from levels 1 to 10. As the patients’ ability to perform the exercise games increased, the therapist gradually challenged them by regulating the objects’ speeds, numbers, intervals, and angles, as appropriate for the patients’ condition, except in the case of the Drum program. Only total beat numbers during treatment were shown on the screen at the end of the Drum program. Each program was performed for 3 mins, with instructions given by the occupational therapist, followed by a break of 2 mins between programs (30 mins total session time). During the 2 mins of interval time, the therapist changed and prepared the next program and performed range of motion exercises with the
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UE of the patient. The patients were asked to mainly use the affected UE, but some of the programs required the use of both UEs. A glove was applied only to the paretic arm. By displaying the points gained on the screen, the therapist provided continuous feedback to the patients during the treatment session.
Evaluation of UE Function Initial evaluations of UE function were performed using the Brunnstrom approach, which comprises six proposed stages of motor power recovery; the Modified Ashworth scale for grading spasticity; as well as the MFT, the BBT, and the FMS. To compare initial motor power of the affected UE, a manual muscle test was performed. On this scale, 0 indicates no function (lack of contraction); 1, trace function (slight contraction with no movement); 2, poor function (full range of motion in the absence of gravity); 3, fair function (full range of
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motion against the gravity); 4, good function (full range of motion, some resistance); and 5, normal function (full range of motion, full resistance). The manual muscle test is the most commonly used evaluation tool for documenting impairment in muscle strength.20 To evaluate gross manual dexterity, the BBT was used.21 The patient was required to grasp one block at a time with his/her affected hand, transport the block over a partition, and place as many blocks as possible into a box on the opposite side within 60 secs; the number of blocks that were successfully moved was counted. The MFT measures gross and fine motor function in the UE on a scale of 0Y32, and its reliability is considered excellent (intraclass correlation coefficient, 0.99).22 Its scores are divided into shoulder/elbow/forearm (S/E/F) and hand dexterity segments, each of which is scored from 0 to 16. The motor subset of the FMS for the UE, which has a scale from 0 to 66, was used to assess sensation, range of motion, reflexes, synergy, as well as fine and gross hand movements; its reliability and validity are considered good (intraclass correlation coefficient, 0.97).23,24 The primary outcome was evaluated by the BBT, the MFT, and the FMS, and the secondary outcome was evaluated by the K-MBI, which was used to assess the activities of daily living. The reliability and the validity of the K-MBI, which was translated by six senior Korean physiatrists using
the fifth version of the MBI, were approved.25 Follow-up evaluations were conducted in all patients by applying the MFT, the BBT, the FMS, and the K-MBI immediately after a 3-wk treatment period. Initial and follow-up evaluations were performed by an experienced occupational therapist who was blinded to the group allocation.
Statistical Analysis All variables were analyzed using the Statistical Package for the Social Sciences, version 18.0 (Statistical Package for the Social Sciences Inc, Chicago, IL). Statistical significance was defined as a P value of less than 0.05. Missing data were dealt with by the simple mean imputation method, whereby the missing value is replaced with the mean of the group. Because the data were not normally distributed, nonparametric tests were conducted. Median values with interquartile range were presented instead of mean values with standard deviation in the data that were not normally distributed. The Wilcoxon’s signed-rank test was used to analyze changes in UE function and activities of daily living over time in each group. The Mann-Whitney U test was used for comparison of assessment score differences between the intervention and control groups (for all subjects and for subjects subdivided into groups of benign/malignant tumor). In addition,
TABLE 1 Demographic and baseline characteristics of the study participants Characteristics Age, yrs Sex (male/female) Type of tumor Meningioma Glioblastoma Low-grade astrocytoma Metastatic tumor Schwannoma Others (PNET, PCNSL) Benign/malignant Location (right/left/both) Disease duration, mos Treatment Resection Resection, CCRT Resection, radiation GKRS Radiation only
Intervention (n = 20)
Control (n = 20)
P
48.6 (11.3) 9:11
50.0 (17.5) 8:12
0.99 0.74
5 5 2 4 1 3 9:11 6:9:5 8.1 (5.5)
4 5 2 4 2 3 11:9 6:8:6 9.8 (6.1)
0.75
9 4 4 2 1
8 6 5 1 0
0.53 0.54 0.33 0.80
Values are given as absolute numbers or as mean (standard deviation). Categorical variables: W2 test or Fisher’s exact test. Continuous variables: Mann-Whitney U test. CCRT, concurrent chemoradiation therapy; GKRS, gamma knife radiation surgery; PCNSL, primary central nervous system lymphoma; PNET, primitive neuroectodermal tumor.
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the Mann-Whitney U test was used for evaluating differences between benign and malignant tumor in the intervention and control groups.
RESULTS Sixty patients with impaired UE motor function as a result of brain tumors were initially evaluated. Thirteen patients were excluded for cognitive impairment, global aphasia, severe shoulder pain on the affected side, and recurred brain tumor. The remaining 47 individuals met this study’s inclusion criteria and were enrolled in the study. Twenty-four patients were assigned to the intervention group (VR-based therapy combined with conventional OT), and 23 patients were assigned to the control group (conventional OT alone). The groups were closely matched according to the participants’ age and type of tumor (Table 1). Four patients in the intervention group and three patients in the control group
dropped out of the study because of various issues, such as tumor progression (two patients in the intervention group), medical problems (two patients in the control group), or unwillingness to continue participation (two patients in the intervention group, one patient in the control group). Finally, a total of 40 patients (20 patients in the intervention group and 20 patients in the control group) completed the study protocol, including follow-up evaluations (Fig. 3). None of the patients in the intervention group expressed fatigue or dissatisfaction with the VR-based therapy. None of the patients in either group reported significant adverse events associated with the overall treatment protocol.
Demographic Details The demographic and baseline characteristics of the study participants did not differ significantly between the two groups (Table 1). The mean Korean
FIGURE 3 Flow chart for subject selection and assignment in this study.
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G0.001 G0.001 0.0010 G0.001 G0.001 0.039 0.347 0.0019 0.134 0.0011
P
version Mini-Mental State Examination scores of the patients were 24.3 in the intervention group and 24.6 in the control group. There was no statistically significant difference.
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40.5 (23.5Y49.8) 84.3 (71.1Y93.8) 39.5 (28.1Y46.8) 37.5 (29.0Y47.3) 60.0 (55.0Y64.0) 35.0 (32.3Y35.8) 8.0 (6.3Y10.0) 9.0 (7.0Y12.8) 4.0 (2.3Y5.4) 73.5 (48.3Y85.5) 34.5 (16.6Y41.0) 72.2 (62.5Y81.6) 35.0 (21.7Y40.0) 31.0 (18.6Y36.7) 53.5 (44.5Y58.3) 32.0 (30.0Y33.8) 8.0 (6.1Y9.8) 8.0 (7.0Y11.8) 3.0 (3.0Y4.0) 54.5 (38.5Y63.7) 30.5 (17.2Y35.5) 70.3 (60.2Y83.6) 33.0 (20.1Y39.8) 33.0 (20.5Y38.6) 52.0 (42.5Y58.3) 31.0 (25.5Y33.0) 7.0 (6.0Y9.8) 7.0 (8.0Y11.8) 3.0 (2.0Y5.1) 52.5 (38.9Y62.8)
38.0 (30.0Y47.3) 82.8 (72.3Y93.8) 39.0 (30.0Y45.1) 38.4 (30.5Y46.5) 58.0 (39.2Y65.5) 34.5 (30.0Y36.0) 7.0 (6.2Y10.0) 8.0 (7.0Y12.6) 4.0 (2.6Y5.6) 70.5 (61.0Y86.3)
G0.001 G0.001 G0.001 G0.001 0.0014 0.048 0.251 0.257 0.052 0.005
Post-Tx Pre-Tx P Post-Tx
Intervention Group (n = 20)
Values are given as median (interquartile range). P by Wilcoxon’s signed-rank test or paired t test with Bonferroni correction. C/S, coordination/speed; H, hand; Tx, treatment; W, wrist.
There were no significant differences in primary outcome and secondary outcome between benign and malignant tumor in each group (Table 4). The
BBT MFT (total score, 0Y100) MFT: S/E/F (0Y50) MFT: H (0Y50) FMS (total score, 0Y66) FMS: S/E/F (0Y36) FMS: W (0Y10) FMS: H (0Y14) FMS: C/S (0Y6) K-MBI
Differences Between Benign and Malignant Tumor
Pre-Tx
There was no significant difference in baseline (pretreatment) K-MBI scores between the two groups. Both of the control and intervention groups demonstrated statistically significant improvements after treatment in K-MBI scores (Table 2). The changes in K-MBI score showed no significant differences between the two groups (Table 3).
Parameter
Secondary Outcome: Activities of Daily Living
TABLE 2 Pretreatment vs. posttreatment parameters in case and control groups
The initial motor power and Brunnstrom stage of the affected UE were similar between the two groups (median values were 3 for UE motor power and 4 for Brunnstrom stage in both groups), and no significant differences were observed in baseline (pretreatment) BBT, MFT, and FMS scores. The differences between before and after treatment in each group were shown in Table 2. The FMS was subdivided for independent assessment of S/E/F (score, 0Y36), wrist (score, 0Y10), and hand function (score, 0Y14) as well as overall coordination/speed of the UE (score, 0Y6). In addition, the MFT was subdivided for independent assessment of S/E/F function (low score, 0Y16) and hand dexterity (low score, 0Y16). Each subsection of the MFT was scored on a scale from 0 to 50 (MFT score in this study = low MFT score 3.125).26 The intervention group showed statistically significant improvement in the BBT compared with the control group. In terms of MFT scores, the intervention group demonstrated significant improvement in the S/E/F subsection of the test relative to the control group. By contrast, the control group showed significant improvement in hand dexterity relative to the intervention group. In terms of FMS scores, the intervention group also demonstrated significant improvement in the S/E/F subsection of the test relative to the control group, whereas the control group continued to exhibit significantly better performance in the hand subsection of the test (Table 3).
Control Group (n = 20)
Primary Outcome: UE Function
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TABLE 3 Comparison of treatment effects between case and control groups Parameter
Intervention Group (n = 20)
Control Group (n = 20)
P
11.0 (9.0Y13.75) 11.0 (9.4Y15.6) 7.0 (6.0Y9.8) 4.0 (3.3Y7.8) 6.5 (4.0Y8.8) 3.5 (2.3Y4.8) 1.0 (0Y2.0) 1.0 (0Y2.0) 1.0 (0Y2.0) 15.0 (10.0Y29.5)
8.0 (6.0Y9.8) 12.5 (9.4Y14.8) 5.0 (2.3Y6.0) 7.5 (5.5Y9.5) 7.0 (5.0Y8.8) 2.0 (2.0Y2.0) 1.0 (0Y2.0) 2.0 (2.0Y3.0) 1.0 (1.0Y2.0) 16.0 (14.3Y22.5)
0.044 90.999 0.007 0.010 90.999 0.012 90.999 0.046 90.999 90.999
¸ BBT ¸ MFT (total score, 0Y100) ¸ MFT: S/E/F (0Y50) ¸ MFT: H (0Y50) ¸ FMS (total score) ¸ FMS: S/E/F (0Y36) ¸ FMS: W (0Y10) ¸ FMS: H (0Y14) ¸ FMS: C/S (0Y6) ¸ K-MBI
Values are given as median (interquartile range). P Mann-Whitney U test with Bonferroni correction. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
authors compared the two groups within the patients with benign and malignant tumor. The intervention group showed more improvement in the S/E/F subsection of the MFT and the FMS, and the control group showed more improvement in the hand subsection of the MFT and the FMS in the patients with benign brain tumor. These findings were also similar in the patients with malignant brain tumor (Table 5).
intervention. The patients in the intervention group improved significantly in proximal UE function, as assessed by a better score on the S/E/F segment of the MFT and the FMS as well as enhanced speed of movement. On the other hand, the patients in the control group showed more improvement in fine motor function and overall coordination as assessed by a better score on the hand segment of the MFT and the FMS.
DISCUSSION
Virtual Reality
The major findings of this study are that VRbased rehabilitation combined with conventional OT is better than the conventional OT alone for UE training in patients with brain tumor. Both groups had significantly improved UE function over time; changes in subscore were different according to the
VR has been successfully used to facilitate upper motor function, which may be related to the enhanced neuroplasticity observed after VR-based rehabilitation.14,27Y31 The use of VR demonstrates the practiced, dependent enhancement of the affected arm by facilitating cortical reorganization.31 As reported
TABLE 4 Comparison of treatment effect between benign and malignant tumor in each group Intervention (n = 20) Parameter
Benign (n = 9)
Malignant (n = 11)
Control (n = 20) P
Benign (n = 11)
Malignant (n = 9)
¸ BBT 9.0 (7.5Y12.5) 11.0 (9Y16) 0.266 8.0 (5Y9) 9.0 (6Y11) ¸ MFT (total score, 0Y100) 9.4 (9.4Y15.6) 15.6 (9.4Y18.8) 0.179 12.5 (12.5Y15.6) 9.4 (9.4Y12.5) ¸ MFT: S/E/F (0Y50) 9.4 (3.1Y12.5) 6.3 (6.3Y12.5) 0.338 6.3 (3.1Y9.4) 6.3 (3.1Y12.5) ¸ MFT: H (0Y50) 3.1 (3.1Y6.3) 3.1 (3.1Y9.4) 0.513 6.3 (3.1Y9.4) 3.1 (3.1Y6.3) ¸ FMS (total score, 0Y66) 5.0 (4.5Y8.5) 7.0 (4Y10) 0.788 6.0 (5Y9) 7.0 (5.5Y8.5) ¸ FMS: S/E/F (0Y36) 3.0 (2.5Y4.5) 4.0 (2Y6) 0.698 2.0 (2Y2) 2.0 (1.5Y2.5) ¸ FMS: W (0Y10) 1.0 (0Y2) 1.0 (0Y2) 0.845 1.0 (0Y2) 2.0 (0Y2) ¸ FMS: H (0Y14) 1.0 (0Y2) 1.0 (0Y2) 0.472 2.0 (2Y3) 2.0 (1.5Y3) ¸ FMS: C/S (0Y6) 1.0 (0.5Y1.5) 1.0 (0Y2) 0.321 1.0 (1Y2) 2.0 (0.5Y2) ¸ K-MBI 25.0 (9Y32.5) 14.0 (10Y28) 0.704 17.0 (12Y24) 16.0 (14.5Y21)
P 0.338 0.179 0.226 0.778 0.513 0.931 0.597 0.841 0.472 0.619
Values are given as median (interquartile range). P by Mann-Whitney U test. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
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TABLE 5 Comparison of treatment effects between case and control groups according to tumor type Benign Tumor (n = 20) Parameter
Intervention (n = 9)
Control (n = 11)
Malignant Tumor (n = 20) P
¸ BBT 9.0 (7.5Y12.5) 8.0 (5Y9) ¸ MFT (total score, 0Y100) 9.4 (9.4Y14.1) 12.5 (12.5Y15.6) ¸ MFT: S/E/F (0Y50) 9.4 (6.3Y12.5) 3.1 (3.1Y12.5) ¸ MFT: H (0Y50) 3.1 (3.1Y9.4) 6.3 (6.3Y15.6) ¸ FMS (total score, 0Y66) 5.0 (4.5Y8.5) 6.0 (5Y9) ¸ FMS: S/E/F (0Y36) 3.0 (2.5Y4.5) 2.0 (2Y2) ¸ FMS: W (0Y10) 1.0 (0Y2) 1.0 (0Y2) ¸ FMS: H (0Y14) 1.0 (0Y2) 2.0 (2Y3) ¸ FMS: C/S (0Y6) 1.0 (0.5Y1.5) 1.0 (1Y2) ¸ K-MBI 25.0 (9Y32.5) 17.0 (12Y24)
Intervention (n = 11)
Control (n = 9)
0.065 11.0 (9Y16) 9.0 (6Y11) 0.186 15.6 (9.4Y18.7) 9.4 (9.4Y12.5) 0.018 6.3 (6.3Y9.4) 3.1 (3.1Y12.5) 0.038 3.1 (3.1Y9.4) 6.3 (6.3Y12.5) 0.535 7.0 (4Y10) 7.0 (5.5Y8.5) 0.018 4.0 (2Y6) 2.0 (1.5Y2.5) 0.871 1.0 (0Y2) 2.0 (0Y2) 0.018 1.0 (0Y2) 2.0 (1.5Y3) 0.706 1.0 (0Y2) 2.0 (0.5Y2) 0.450 14.0 (10Y28) 16.0 (14.5Y21)
P 0.056 0.197 0.026 0.040 0.639 0.015 0.576 0.041 0.161 0.621
Values are given as median (interquartile range). P by Mann-Whitney U test. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
in recent studies, whether adding VR programs to conventional therapy facilitates patient progress remains to be determined.11,27 Piron et al.32 found that patients with subacute stroke who received supplemental VR therapy showed more improvements in the FMS and the Functional Independence Measure scale than did patients with subacute stroke who received only conventional therapy. The results of Piron and colleagues are therefore similar to this study’s observations. On the other hand, Crosbie et al.33 concluded that VR-based therapy had no significant effect on UE function or activity levels compared with conventional rehabilitation in patients with chronic stroke.33 By contrast, Mumford et al.34 demonstrated that VR therapy (performed for 1 hr per session for 12 sessions during the course of 4 wks) in addition to conventional physical therapy improved upper limb motor control in nine patients with traumatic brain injury. There have been several studies to clarify the effect of VR-based rehabilitation on UE function, but reported results are not consistent. On this study’s results, VR-based rehabilitation possibly demonstrates significant improvements especially in the proximal UE. This observation might stem from the authors’ selection of VR programs that mostly facilitate proximal UE recovery. The application of VR programs that instead facilitate hand movement and dexterity might considerably alter the results of this study. Conversely, the patients who received conventional OT showed more improvements in hand function. This phenomenon may be a result of fine motor training occupying one-third of the conventional OT session. For patients with proximal UE and distal UE dysfunction www.ajpmr.com
of similar degree, the addition of a VR program to conventional OT will have the advantage of improving overall UE function. The patients who received VR-based rehabilitation demonstrated improvements in K-MBI scores that were similar to the control group (21.7 [17.6] vs. 22.1 [19.5]). The authors hypothesize that the lack of superiority in the intervention group is because most of the motions in the VR programs primarily required movements of the shoulder and the elbow. Common activities of daily life require not only proximal UE movements but also fine hand movements, such as gripping objects (combs, spoons, and chopsticks) and fastening buttons. However, shoulder flexor, abductor, external rotator, internal rotator, elbow flexor, and extensor were required for activities of daily living such as washing up, combing the hair, feeding, dressing, and chair/bed transfer. The authors thought that VR-based rehabilitation can be more helpful for these muscle movements according to the S/E/F score of the FMS and the MFT. In the current study, VR therapy was conducted in the form of games, with continuous instructions and encouragement from the therapist, accompanied by various background music and ongoing visual and tactile stimulation. The authors hypothesize that these conditions offered interest, and patients can more actively participate in rehabilitation than conventional OT. The VR program also provides continuous real-time feedback regarding the patients’ performance, with their scores displayed on the television monitor or by the therapist. As demonstrated previously,35 these conditions allowed the study participants to immediately correct any errors of their motion promptly. Taken Virtual Reality–Based Rehabilitation on UE Function
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together, provision of interest, real-time feedback and task-oriented training, repetition of similar motions, as well as matching the VR intensity level with the individual’s abilities all most likely lent themselves to the recovery of UE motor function by promoting cortical reorganization. No adverse events were documented during the course of this investigation. Most of the participants in the intervention group reported that the VR tasks were easy to understand. Furthermore, the participants indicated their satisfaction with the conduct of the trial, and only two persons in the VR group stated that they did not enjoy the experience. Two patients made complaints about the composition of the programs used in the treatment session.
of the UE-FMS ranged from 4.25 to 7.25 points, depending on the different facets of UE movement with chronic stroke patients.36 The minimum clinically important difference of the MBI is 1.85 points in patients with acute stroke.37 Unlike for patients with stroke, the minimum clinically important difference of the FMS and the K-MBI has not been established for patients with brain tumor. Lastly, none of the current VR programs in the IREX System target hand movement, and the glove itself worn by the patients was recognized by a video camera during the VR training in this study, so they cannot use fingers during treatment session. Further studies considering hand function as well as the development and use of VR programs targeting hand use are required for patients with brain tumor.
Strengths and Limitations of the Study and Suggestions for Future Research
CONCLUSIONS
This is the first study designed to investigate the effect of VR-based rehabilitation combined with conventional OT for improving UE function in patients with brain tumor. The authors recruited patients with motor power in the affected arm that was higher than poor grade because patients with functional level poorer than this cannot capable of activities within the IREX System and excluded patients with recurred brain tumor, thus increasing homogeneity. The authors additionally analyzed the subsegment of the MFT and the FMS that provided more detailed information regarding UE function for each segment. However, this study has several limitations for consideration in future studies. First, this study was not a randomized controlled trial, had a small sample size, and was unable to determine the longterm effect of VR therapy. Further randomized controlled trials that include a large number of patients and long-term follow-up are thus required to fully evaluate the therapeutic potential of VR for patients with brain tumor. Second, baseline K-MBI scores were slightly lower in the intervention group than in the control group. However, there was no statistically significant difference. Third, cognitive deficits, sensory loss, and other medical issues that could influence the functional outcomes of this work were not taken into account in this study’s results. Fourth, minimum clinically important difference for each assessment used was not described in this study. Minimum clinically important difference for the BBT and the MFT has not been established in not only patients with stroke but also patients with brain tumor. Estimated clinically important difference
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The results of the current study demonstrate that VR-based rehabilitation and conventional OT are both effective treatments for the improvement in UE function in patients with brain tumor. VRbased rehabilitation combined with conventional OT may be more successful than conventional OT, especially for the restoration of proximal UE dysfunction. This effectiveness may be applied similarly to patients with benign and malignant tumor. In addition to its ample feasibility for application to patients with brain tumor, VR therapy is safe, well tolerated, and helpful for functional UE recovery in patients with brain tumor.
REFERENCES 1. Salander P, Spetz A: How do patients and spouses deal with the serious facts of malignant glioma? Palliat Med 2002;16:305Y13 2. O’Dell MW, Barr K, Spanier D, et al: Functional outcome of inpatient rehabilitation in persons with brain tumors. Arch Phys Med Rehabil 1998;79:1530Y4 3. Tang V, Rathbone M, Park Dorsay J, et al: Rehabilitation in primary and metastatic brain tumours: Impact of functional outcomes on survival. J Neurol 2008;255:820Y7 4. Greenberg E, Treger I, Ring H: Rehabilitation outcomes in patients with brain tumors and acute stroke: Comparative study of inpatient rehabilitation. Am J Phys Med Rehabil 2006;85:568Y73 5. Marciniak CM, Sliwa JA, Heinemann AW, et al: Functional outcomes of persons with brain tumors after inpatient rehabilitation. Arch Phys Med Rehabil 2001; 82:457Y63 6. Cole RP, Scialla SJ, Bednarz L: Functional recovery in cancer rehabilitation. Arch Phys Med Rehabil 2000; 81:623Y7
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7. Marciniak CM, Sliwa JA, Spill G, et al: Functional outcome following rehabilitation of the cancer patient. Arch Phys Med Rehabil 1996;77:54Y7
23. Alonso-Alonso M, Fregni F, Pascual-Leone A: Brain stimulation in poststroke rehabilitation. Cerebrovasc Dis 2007;24:157Y66
8. Huang ME, Cifu DX, Keyser-Marcus L: Functional outcome after brain tumor and acute stroke: A comparative analysis. Arch Phys Med Rehabil 1998;79:1386Y90
24. Fugl-Meyer AR, Ja¨a¨sko¨ L, Leyman I, et al: The poststroke hemiplegic patient. 1. A method for evaluation of physical performance. Scand J Rehabil Med 1975;7:13Y31
9. Lam YS, Man DW, Tam SF, et al: Virtual reality training for stroke rehabilitation. NeuroRehabilitation 2006;21:245Y53 10. Sung WH, Chiu TY, Tsai WW, et al: The effect of virtual realityYenhanced driving protocol in patients following spinal cord injury. J Chin Med Assoc 2012;75:600Y5 11. Lucca LF: Virtual reality and motor rehabilitation of the upper limb after stroke: A generation of progress? J Rehabil Med 2009;41:1003Y100 12. Mirelman A, Maidan I, Herman T, et al: Virtual reality for gait training: Can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? J Gerontol A Biol Sci Med Sci 2011;66:234Y40 13. Kim BR, Chun MH, Kim LS, et al: Effect of virtual reality on cognition in stroke patients. Ann Rehabil Med 2011;35:450Y9 14. Jang SH, You SH, Hallett M, et al: Cortical reorganization and associated functional motor recovery after virtual reality in patients with chronic stroke: An experimenter-blind preliminary study. Arch Phys Med Rehabil 2005;86:2218Y23 15. Fischer HC, Stubblefield K, Kline T, et al: Hand rehabilitation following stroke: A pilot study of assisted finger extension training in a virtual environment. Top Stroke Rehabil 2007;14:1Y12 16. Albert ML: A simple test of visual neglect. Neurology 1973;23:658Y64 17. Han C, Jo SA, Jo I, et al: An adaptation of the Korean Mini-Mental State Examination (K-MMSE) in elderly Koreans: Demographic influence and populationbased norms (the AGE study). Arch Gerontol Geriatr 2008;47:302Y10 18. Winstein CJ, Rose DK, Tan SM, et al: A randomized controlled comparison of upper-extremity rehabilitation strategies in acute stroke: A pilot study of immediate and long-term outcomes. Arch Phys Med Rehabil 2004;85:620Y8 19. Platz T, Winter T, Muller N, et al: Arm ability training for stroke and traumatic brain injury patients with mild arm paresis: A single-blind, randomized, controlled trial. Arch Phys Med Rehabil 2001;82:961Y8 20. Cuthbert SC, Goodheart GJ Jr: On the reliability and validity of manual muscle testing: A literature review. Chiropr Osteopat 2007;15:4
25. Jung HY, Park BK, Shin HS, et al: Development of the Korean version of Modified Barthel Index (K-MBI): Multi-center study for subjects with stroke. J Korean Acad Rehabil Med 2007;31:283Y97 26. Nakamura R, Moriyama S: Manual Function Test(MFT) and Functional Occupational Therapy for Stroke Patients. Saitama, Japan, National Rehabilitation Center for the Disabled, 2000 27. Langhorne P, Coupar F, Pollock A: Motor recovery after stroke: A systematic review. Lancet Neurol 2009; 8:741Y54 28. Saposnik G, Levin M; Outcome Research Canada Working Group: Virtual reality in stroke rehabilitation: A meta-analysis and implications for clinicians. Stroke 2011;42:1380Y6 29. Saposnik G, Teasell R, Mamdani M, et al: Effectiveness of virtual reality using Wii gaming technology in stroke rehabilitation: A pilot randomized clinical trial and proof of principle. Stroke 2010; 41:1477Y84 30. Henderson A, Korner-Bitensky N, Levin M: Virtual reality in stroke rehabilitation: A systematic review of its effectiveness for upper limb motor recovery. Top Stroke Rehabil 2007;14:52Y61 31. Kleim JA, Jones TA: Principles of experiencedependent neural plasticity: Implications for rehabilitation after brain damage. J Speech Lang Hear Res 2008;51:S225Y39 32. Piron L, Turolla A, Agostini M, et al: Exercises for paretic upper limb after stroke: A combined virtualreality and telemedicine approach. J Rehabil Med 2009;41:1016Y102 33. Crosbie JH, Lennon S, McGoldrick MC, et al: Virtual reality in the rehabilitation of the arm after hemiplegic stroke: A randomized controlled pilot study. Clin Rehabil 2012;26:798Y806 34. Mumford N, Duckworth J, Thomas PR, et al: Upperlimb virtual rehabilitation for traumatic brain injury: A preliminary within-group evaluation of the elements system. Brain Inj 2012;26:166Y76 35. Duncan PW, Zorowitz R, Bates B, et al: Management of adult stroke rehabilitation care: A clinical practice guideline. Stroke 2005;36:e100Y43
21. Mathiowetz V, Volland G, Kashman N, et al: Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 1985;39:386Y91
36. Page SJ, Fulk GD, Boyne P: Clinically important differences for the upper-extremity Fugl-Meyer Scale in people with minimal to moderate impairment due to chronic stroke. Phys Ther 2012;92:791Y8
22. Nakamura R, Moriyama S, Yamada Y, et al: Recovery of impaired motor function of the upper extremity after stroke. Tohoku J Exp Med 1992; 168:11Y20
37. Hsieh YW, Wang CH, Wu SC, et al: Establishing the minimal clinically important difference of the Barthel Index in stroke patients. Neurorehabil Neural Repair 2007;21:233Y8
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Affiliations: From the Department of Rehabilitation Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul (JY, MHC); Department of Physical Medicine and Rehabilitation, Dong-A University College of Medicine, Busan (SJL); and Department of Rehabilitation Medicine, Jeju National University Hospital, University of Jeju College of Medicine, Jeju, Republic of Korea (BRK).
ORIGINAL RESEARCH ARTICLE
Effect of Virtual RealityYBased Rehabilitation on Upper-Extremity Function in Patients with Brain Tumor Controlled Trial
Correspondence: All correspondence and requests for reprints should be addressed to: Min Ho Chun, MD, PhD, Department of Rehabilitation Medicine, Asan Medical Center, University of Ulsan College of Medicine, 88, Olympic-Ro 43-Gil, Songpa-gu, Seoul 138Y736, Republic of Korea.
ABSTRACT Yoon J, Chun MH, Lee SJ, Kim BR: Effect of virtual realityYbased rehabilitation on upper-extremity function in patients with brain tumor: controlled trial. Am J Phys Med Rehabil 2015;94:449Y459.
Objective: The aim of this study was to evaluate the benefit of virtual realityYbased rehabilitation on upper-extremity function in patients with brain tumor.
Disclosures:
Design: Patients with upper-extremity dysfunction were divided into age-
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
matched and tumor typeYmatched two groups. The intervention group performed the virtual reality program 30 mins per session for 9 sessions and conventional occupational therapy 30 mins per session for 6 sessions for 3 wks, whereas the control group received conventional occupational therapy alone 30 mins per session for 15 sessions for 3 wks. The Box and Block test, the Manual Function test, and the Fugl-Meyer scale were used to evaluate upper-extremity function. The Korean version of the Modified Barthel Index was used to assess activities of daily living.
Results: Forty patients completed the study (20 for each group). Each group 0894-9115/15/9406-0449 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/PHM.0000000000000192
exhibited significant posttreatment improvements in the Box and Block test, Manual Function test, Fugl-Meyer scale, and Korean version of the Modified Barthel Index scores. The Box and Block test, the Fugl-Meyer scale, and the Manual Function test showed greater improvements in shoulder/elbow/forearm function in the intervention group and hand function in the control group.
Conclusions: Virtual realityYbased rehabilitation combined with conventional occupational therapy may be more effective than conventional occupational therapy, especially for proximal upper-extremity function in patients with brain tumor. Further studies considering hand function, such as use of virtual reality programs that targeting hand use, are required. Key Words:
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Brain Tumor, Upper-Extremity Function, Virtual Reality, Occupational Therapy
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P
rimary brain tumors account for less than 2% of all malignancies and generally leave the affected patient with significant functional impairment.1,2 Aggressive treatments based on surgery, radiation, and chemotherapy frequently lead to improved survival rates for patients with brain tumors. Nonetheless, brain tumors continue to cause pronounced neurologic deficits despite these interventions. Cognitive impairment is the most commonly reported deficit, at an occurrence rate of 80%, followed by motor weakness (78%), visual-perceptual deficits (53%), sensory loss (38%), and bowel and/or bladder dysfunction (37%). The neurologic impairments are similar to those found in patients who have had a stroke or a traumatic brain injury.3 Rehabilitation therapy in patients with brain tumor has gained prominence during the past three decades, and several studies indicated that individuals with brain tumors make significant functional strides after rehabilitation.4Y7 For example, Huang et al.8 demonstrated that patients with brain tumor in acute inpatient rehabilitation centers had a decreased length of stay compared with patients with stroke and also achieved functional gains comparable with those of stroke survivors. Along the same lines, O’Dell et al.2 found that brain tumor patients with appropriate rehabilitative treatment achieved functional gains approaching those of patients with brain injury. Virtual reality (VR) can be defined as the Buse of interactive simulations created with computer hardware and software to present users with opportunities to engage in environments that appear and feel similar to real-world objects and events.[9 VR programs are used in various kinds of vocational training, including flight simulations for pilots and driving simulations for automobile operators.10 Recently, VR programs have also been incorporated into neurologic rehabilitation agenda to improve upper-extremity (UE) function,11 lower extremity function,12 and gait.12 In addition, VR is widely used in the field of brain disease for cognitive rehabilitation.13 Heretofore, most investigations of VR therapy have been directed toward improving motor function in patients with stroke and traumatic brain injuries. Several randomized controlled trials have compared VR-mediated therapy with conventional occupational therapy (OT) for the enhancement of UE function and have shown significant improvements in the Box and Block test (BBT) of manual dexterity, the Fugl-Meyer scale (FMS), the Manual Function test (MFT), and the Wolf Motor Function test score of UE motor ability.14,15
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To the best of the authors’ knowledge, no investigations have been performed to date regarding the effect of VR-based rehabilitation on the restoration of UE function in patients with brain tumor. The aim of this study was to evaluate the ability of VR-based rehabilitation to improve hand, arm, and shoulder function in these individuals. The primary outcome of this study was an improvement in UE function evaluated by the BBT, the MFT, and the FMS. The secondary outcome was an improvement in activities of daily living evaluated by the Korean version of the Modified Barthel Index (K-MBI). The authors hypothesized that combining VR-based rehabilitation with conventional OT would help to improve UE function in patients with brain tumor compared with conventional OT.
METHODS Study Participants Patients with UE dysfunction as a consequence of brain tumor were recruited from an inpatient clinic in the Department of Rehabilitation Medicine of the Asan Medical Center, Seoul, Republic of Korea, from March 1, 2011, through March 1, 2012. Inclusion criteria were as follows: (1) a brain tumor diagnosis with a stable status after the completion of proper management (surgery, chemotherapy, or radiation therapy); (2) patients with a Korean version Mini-Mental State Examination score of greater than 20 who are capable of understanding the therapist’s instructions; (3) a Brunnstrom stage of higher than 2 (2: hyperreflexia, emergence of spasticity and synergies, minimal voluntary movement in the affected limbs) corresponding to the affected UE; (4) a score on the Modified Ashworth spasticity scale of less than 2 (2: more marked increase in muscle tone through most of the range of motion but affected part is easily moved); and (5) motor power grade of the affected shoulder of higher than Bpoor[ (poor strength corresponds to inability to perform movements against gravity but complete range of motion when the pull of gravity is eliminated). Exclusion criteria were as follows: (1) a diagnosis of global aphasia; (2) decreased sitting balance; (3) a recurrent brain tumor; (4) perceptualcognitive dysfunction (visuospatial neglect and cognitive function evaluated by the Albert test16 and the Korean version Mini-Mental State Examination17); (5) musculoskeletal problems and/or peripheral neuropathy of the affected limb; and (6) medical instability (acute inflammation or infection such as pneumonia, urinary tract infection, and sepsis).
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The patients were allocated into two groups by developing the stratified random sampling numbers by dividing strata using two variables (age, type of tumor). All participants provided written informed consent before the initiation of the study. The study protocol was approved by the Research Ethics Committee of the Asan Medical Center.
Study Protocol The individuals in the intervention group carried out the VR programs described below for 3 wks at a frequency of 30 mins per day, three times per week (nine sessions). The patients in the intervention group also received conventional OT for 3 wks at a frequency of 30 mins per day, two times per week (6 sessions), whereas the control group received conventional OT alone for 3 wks at a frequency of 30 mins per day, five times per week (15 sessions). For the duration of this study, all participants received conventional rehabilitation including physical, occupational, and cognitive therapies of the same intensity and duration. Conventional OT consisted of range of motion exercises, fine motor training, and strengthening UE exercises.18 Range of motion exercises consisted of overhead pulley, range of motion arc, and inserting rings to a horizontal bar. Fine motor training consisted of turning coins, tapping of the thumb and the index finger, as well as inserting a piece of wood into small holes in a pegboard.19 Strengthening exercises consisted of upper body exerciser, sanding, weight pulley exercises, and using a Theraband or lifting a dumbbell. Each exercise took approximately 10 mins. VR-based rehabilitation was performed by an occupational therapist proficient in the use of the Interactive Rehabilitation and Exercise (IREX) Sys-
tem (Vivid Group, Toronto, Canada), described below (GestureTek Health, IREX). Therapists were blinded to the study design. The IREX System VR environment entails a television monitor, a video camera, a computer recognition glove, virtual objects, and a number of VR programs (Fig. 1). Video cameras placed the patients within the VR environment by analyzing their positions and movements. Computer recognition gloves also read the patients’ reactions (responsive movements) and transferred them to the VR system. The patient was able to see his/her own body movement in real time, which allowed the patient to be immersed inside the virtual environment. Six VR programs (Birds and Balls, Conveyor, Drums, Juggler, Coconuts, and Soccer) were selected from a total of 20 available programs (Fig. 2). The Birds and Balls program involves balls appearing on the screen from various directions. The balls burst into birds when the patient touches them by using his/her hand movements. The Coconuts program denotes a basket that moves from the left or the right across the screen in response to the patient’s arm movements. The aim of the game is to use the basket to catch the coconuts falling from the upper portion of the screen. The Conveyor program depicts two conveyor belts located at the left and the right hand side of the screen, with boxes appearing from either side. Patients are asked to use their hand movements to shift the boxes from one conveyer belt to the other. The Juggler program requires the patient to keep several balls simultaneously moving in the air with his/her hands. The Drum program asks the patient to use his/her hands to play a drum along with the rhythm of music. Finally, the Soccer program depicts a soccer ball flying toward the patient, who is asked to stop the ball by using his/her hand as a goalkeeper. These
FIGURE 1 The virtual reality experimental setup of the IREX System (Vivid Group, Toronto, Canada). www.ajpmr.com
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FIGURE 2 Six VR programs used in this study. A, birds and balls; B, conveyor; C, drums; D, juggler; E, coconuts; F, soccer.
six programs specifically demand UE movements such as shoulder flexor/adductor/abductor, elbow flexor, or elbow extensor muscles and can be performed in a standing position or a sitting position. Each program provided background music related to the game. Degrees of difficulty were set by the therapist or by the request of the patient, ranging from levels 1 to 10. As the patients’ ability to perform the exercise games increased, the therapist gradually challenged them by regulating the objects’ speeds, numbers, intervals, and angles, as appropriate for the patients’ condition, except in the case of the Drum program. Only total beat numbers during treatment were shown on the screen at the end of the Drum program. Each program was performed for 3 mins, with instructions given by the occupational therapist, followed by a break of 2 mins between programs (30 mins total session time). During the 2 mins of interval time, the therapist changed and prepared the next program and performed range of motion exercises with the
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UE of the patient. The patients were asked to mainly use the affected UE, but some of the programs required the use of both UEs. A glove was applied only to the paretic arm. By displaying the points gained on the screen, the therapist provided continuous feedback to the patients during the treatment session.
Evaluation of UE Function Initial evaluations of UE function were performed using the Brunnstrom approach, which comprises six proposed stages of motor power recovery; the Modified Ashworth scale for grading spasticity; as well as the MFT, the BBT, and the FMS. To compare initial motor power of the affected UE, a manual muscle test was performed. On this scale, 0 indicates no function (lack of contraction); 1, trace function (slight contraction with no movement); 2, poor function (full range of motion in the absence of gravity); 3, fair function (full range of
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motion against the gravity); 4, good function (full range of motion, some resistance); and 5, normal function (full range of motion, full resistance). The manual muscle test is the most commonly used evaluation tool for documenting impairment in muscle strength.20 To evaluate gross manual dexterity, the BBT was used.21 The patient was required to grasp one block at a time with his/her affected hand, transport the block over a partition, and place as many blocks as possible into a box on the opposite side within 60 secs; the number of blocks that were successfully moved was counted. The MFT measures gross and fine motor function in the UE on a scale of 0Y32, and its reliability is considered excellent (intraclass correlation coefficient, 0.99).22 Its scores are divided into shoulder/elbow/forearm (S/E/F) and hand dexterity segments, each of which is scored from 0 to 16. The motor subset of the FMS for the UE, which has a scale from 0 to 66, was used to assess sensation, range of motion, reflexes, synergy, as well as fine and gross hand movements; its reliability and validity are considered good (intraclass correlation coefficient, 0.97).23,24 The primary outcome was evaluated by the BBT, the MFT, and the FMS, and the secondary outcome was evaluated by the K-MBI, which was used to assess the activities of daily living. The reliability and the validity of the K-MBI, which was translated by six senior Korean physiatrists using
the fifth version of the MBI, were approved.25 Follow-up evaluations were conducted in all patients by applying the MFT, the BBT, the FMS, and the K-MBI immediately after a 3-wk treatment period. Initial and follow-up evaluations were performed by an experienced occupational therapist who was blinded to the group allocation.
Statistical Analysis All variables were analyzed using the Statistical Package for the Social Sciences, version 18.0 (Statistical Package for the Social Sciences Inc, Chicago, IL). Statistical significance was defined as a P value of less than 0.05. Missing data were dealt with by the simple mean imputation method, whereby the missing value is replaced with the mean of the group. Because the data were not normally distributed, nonparametric tests were conducted. Median values with interquartile range were presented instead of mean values with standard deviation in the data that were not normally distributed. The Wilcoxon’s signed-rank test was used to analyze changes in UE function and activities of daily living over time in each group. The Mann-Whitney U test was used for comparison of assessment score differences between the intervention and control groups (for all subjects and for subjects subdivided into groups of benign/malignant tumor). In addition,
TABLE 1 Demographic and baseline characteristics of the study participants Characteristics Age, yrs Sex (male/female) Type of tumor Meningioma Glioblastoma Low-grade astrocytoma Metastatic tumor Schwannoma Others (PNET, PCNSL) Benign/malignant Location (right/left/both) Disease duration, mos Treatment Resection Resection, CCRT Resection, radiation GKRS Radiation only
Intervention (n = 20)
Control (n = 20)
P
48.6 (11.3) 9:11
50.0 (17.5) 8:12
0.99 0.74
5 5 2 4 1 3 9:11 6:9:5 8.1 (5.5)
4 5 2 4 2 3 11:9 6:8:6 9.8 (6.1)
0.75
9 4 4 2 1
8 6 5 1 0
0.53 0.54 0.33 0.80
Values are given as absolute numbers or as mean (standard deviation). Categorical variables: W2 test or Fisher’s exact test. Continuous variables: Mann-Whitney U test. CCRT, concurrent chemoradiation therapy; GKRS, gamma knife radiation surgery; PCNSL, primary central nervous system lymphoma; PNET, primitive neuroectodermal tumor.
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the Mann-Whitney U test was used for evaluating differences between benign and malignant tumor in the intervention and control groups.
RESULTS Sixty patients with impaired UE motor function as a result of brain tumors were initially evaluated. Thirteen patients were excluded for cognitive impairment, global aphasia, severe shoulder pain on the affected side, and recurred brain tumor. The remaining 47 individuals met this study’s inclusion criteria and were enrolled in the study. Twenty-four patients were assigned to the intervention group (VR-based therapy combined with conventional OT), and 23 patients were assigned to the control group (conventional OT alone). The groups were closely matched according to the participants’ age and type of tumor (Table 1). Four patients in the intervention group and three patients in the control group
dropped out of the study because of various issues, such as tumor progression (two patients in the intervention group), medical problems (two patients in the control group), or unwillingness to continue participation (two patients in the intervention group, one patient in the control group). Finally, a total of 40 patients (20 patients in the intervention group and 20 patients in the control group) completed the study protocol, including follow-up evaluations (Fig. 3). None of the patients in the intervention group expressed fatigue or dissatisfaction with the VR-based therapy. None of the patients in either group reported significant adverse events associated with the overall treatment protocol.
Demographic Details The demographic and baseline characteristics of the study participants did not differ significantly between the two groups (Table 1). The mean Korean
FIGURE 3 Flow chart for subject selection and assignment in this study.
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G0.001 G0.001 0.0010 G0.001 G0.001 0.039 0.347 0.0019 0.134 0.0011
P
version Mini-Mental State Examination scores of the patients were 24.3 in the intervention group and 24.6 in the control group. There was no statistically significant difference.
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40.5 (23.5Y49.8) 84.3 (71.1Y93.8) 39.5 (28.1Y46.8) 37.5 (29.0Y47.3) 60.0 (55.0Y64.0) 35.0 (32.3Y35.8) 8.0 (6.3Y10.0) 9.0 (7.0Y12.8) 4.0 (2.3Y5.4) 73.5 (48.3Y85.5) 34.5 (16.6Y41.0) 72.2 (62.5Y81.6) 35.0 (21.7Y40.0) 31.0 (18.6Y36.7) 53.5 (44.5Y58.3) 32.0 (30.0Y33.8) 8.0 (6.1Y9.8) 8.0 (7.0Y11.8) 3.0 (3.0Y4.0) 54.5 (38.5Y63.7) 30.5 (17.2Y35.5) 70.3 (60.2Y83.6) 33.0 (20.1Y39.8) 33.0 (20.5Y38.6) 52.0 (42.5Y58.3) 31.0 (25.5Y33.0) 7.0 (6.0Y9.8) 7.0 (8.0Y11.8) 3.0 (2.0Y5.1) 52.5 (38.9Y62.8)
38.0 (30.0Y47.3) 82.8 (72.3Y93.8) 39.0 (30.0Y45.1) 38.4 (30.5Y46.5) 58.0 (39.2Y65.5) 34.5 (30.0Y36.0) 7.0 (6.2Y10.0) 8.0 (7.0Y12.6) 4.0 (2.6Y5.6) 70.5 (61.0Y86.3)
G0.001 G0.001 G0.001 G0.001 0.0014 0.048 0.251 0.257 0.052 0.005
Post-Tx Pre-Tx P Post-Tx
Intervention Group (n = 20)
Values are given as median (interquartile range). P by Wilcoxon’s signed-rank test or paired t test with Bonferroni correction. C/S, coordination/speed; H, hand; Tx, treatment; W, wrist.
There were no significant differences in primary outcome and secondary outcome between benign and malignant tumor in each group (Table 4). The
BBT MFT (total score, 0Y100) MFT: S/E/F (0Y50) MFT: H (0Y50) FMS (total score, 0Y66) FMS: S/E/F (0Y36) FMS: W (0Y10) FMS: H (0Y14) FMS: C/S (0Y6) K-MBI
Differences Between Benign and Malignant Tumor
Pre-Tx
There was no significant difference in baseline (pretreatment) K-MBI scores between the two groups. Both of the control and intervention groups demonstrated statistically significant improvements after treatment in K-MBI scores (Table 2). The changes in K-MBI score showed no significant differences between the two groups (Table 3).
Parameter
Secondary Outcome: Activities of Daily Living
TABLE 2 Pretreatment vs. posttreatment parameters in case and control groups
The initial motor power and Brunnstrom stage of the affected UE were similar between the two groups (median values were 3 for UE motor power and 4 for Brunnstrom stage in both groups), and no significant differences were observed in baseline (pretreatment) BBT, MFT, and FMS scores. The differences between before and after treatment in each group were shown in Table 2. The FMS was subdivided for independent assessment of S/E/F (score, 0Y36), wrist (score, 0Y10), and hand function (score, 0Y14) as well as overall coordination/speed of the UE (score, 0Y6). In addition, the MFT was subdivided for independent assessment of S/E/F function (low score, 0Y16) and hand dexterity (low score, 0Y16). Each subsection of the MFT was scored on a scale from 0 to 50 (MFT score in this study = low MFT score 3.125).26 The intervention group showed statistically significant improvement in the BBT compared with the control group. In terms of MFT scores, the intervention group demonstrated significant improvement in the S/E/F subsection of the test relative to the control group. By contrast, the control group showed significant improvement in hand dexterity relative to the intervention group. In terms of FMS scores, the intervention group also demonstrated significant improvement in the S/E/F subsection of the test relative to the control group, whereas the control group continued to exhibit significantly better performance in the hand subsection of the test (Table 3).
Control Group (n = 20)
Primary Outcome: UE Function
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TABLE 3 Comparison of treatment effects between case and control groups Parameter
Intervention Group (n = 20)
Control Group (n = 20)
P
11.0 (9.0Y13.75) 11.0 (9.4Y15.6) 7.0 (6.0Y9.8) 4.0 (3.3Y7.8) 6.5 (4.0Y8.8) 3.5 (2.3Y4.8) 1.0 (0Y2.0) 1.0 (0Y2.0) 1.0 (0Y2.0) 15.0 (10.0Y29.5)
8.0 (6.0Y9.8) 12.5 (9.4Y14.8) 5.0 (2.3Y6.0) 7.5 (5.5Y9.5) 7.0 (5.0Y8.8) 2.0 (2.0Y2.0) 1.0 (0Y2.0) 2.0 (2.0Y3.0) 1.0 (1.0Y2.0) 16.0 (14.3Y22.5)
0.044 90.999 0.007 0.010 90.999 0.012 90.999 0.046 90.999 90.999
¸ BBT ¸ MFT (total score, 0Y100) ¸ MFT: S/E/F (0Y50) ¸ MFT: H (0Y50) ¸ FMS (total score) ¸ FMS: S/E/F (0Y36) ¸ FMS: W (0Y10) ¸ FMS: H (0Y14) ¸ FMS: C/S (0Y6) ¸ K-MBI
Values are given as median (interquartile range). P Mann-Whitney U test with Bonferroni correction. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
authors compared the two groups within the patients with benign and malignant tumor. The intervention group showed more improvement in the S/E/F subsection of the MFT and the FMS, and the control group showed more improvement in the hand subsection of the MFT and the FMS in the patients with benign brain tumor. These findings were also similar in the patients with malignant brain tumor (Table 5).
intervention. The patients in the intervention group improved significantly in proximal UE function, as assessed by a better score on the S/E/F segment of the MFT and the FMS as well as enhanced speed of movement. On the other hand, the patients in the control group showed more improvement in fine motor function and overall coordination as assessed by a better score on the hand segment of the MFT and the FMS.
DISCUSSION
Virtual Reality
The major findings of this study are that VRbased rehabilitation combined with conventional OT is better than the conventional OT alone for UE training in patients with brain tumor. Both groups had significantly improved UE function over time; changes in subscore were different according to the
VR has been successfully used to facilitate upper motor function, which may be related to the enhanced neuroplasticity observed after VR-based rehabilitation.14,27Y31 The use of VR demonstrates the practiced, dependent enhancement of the affected arm by facilitating cortical reorganization.31 As reported
TABLE 4 Comparison of treatment effect between benign and malignant tumor in each group Intervention (n = 20) Parameter
Benign (n = 9)
Malignant (n = 11)
Control (n = 20) P
Benign (n = 11)
Malignant (n = 9)
¸ BBT 9.0 (7.5Y12.5) 11.0 (9Y16) 0.266 8.0 (5Y9) 9.0 (6Y11) ¸ MFT (total score, 0Y100) 9.4 (9.4Y15.6) 15.6 (9.4Y18.8) 0.179 12.5 (12.5Y15.6) 9.4 (9.4Y12.5) ¸ MFT: S/E/F (0Y50) 9.4 (3.1Y12.5) 6.3 (6.3Y12.5) 0.338 6.3 (3.1Y9.4) 6.3 (3.1Y12.5) ¸ MFT: H (0Y50) 3.1 (3.1Y6.3) 3.1 (3.1Y9.4) 0.513 6.3 (3.1Y9.4) 3.1 (3.1Y6.3) ¸ FMS (total score, 0Y66) 5.0 (4.5Y8.5) 7.0 (4Y10) 0.788 6.0 (5Y9) 7.0 (5.5Y8.5) ¸ FMS: S/E/F (0Y36) 3.0 (2.5Y4.5) 4.0 (2Y6) 0.698 2.0 (2Y2) 2.0 (1.5Y2.5) ¸ FMS: W (0Y10) 1.0 (0Y2) 1.0 (0Y2) 0.845 1.0 (0Y2) 2.0 (0Y2) ¸ FMS: H (0Y14) 1.0 (0Y2) 1.0 (0Y2) 0.472 2.0 (2Y3) 2.0 (1.5Y3) ¸ FMS: C/S (0Y6) 1.0 (0.5Y1.5) 1.0 (0Y2) 0.321 1.0 (1Y2) 2.0 (0.5Y2) ¸ K-MBI 25.0 (9Y32.5) 14.0 (10Y28) 0.704 17.0 (12Y24) 16.0 (14.5Y21)
P 0.338 0.179 0.226 0.778 0.513 0.931 0.597 0.841 0.472 0.619
Values are given as median (interquartile range). P by Mann-Whitney U test. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
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TABLE 5 Comparison of treatment effects between case and control groups according to tumor type Benign Tumor (n = 20) Parameter
Intervention (n = 9)
Control (n = 11)
Malignant Tumor (n = 20) P
¸ BBT 9.0 (7.5Y12.5) 8.0 (5Y9) ¸ MFT (total score, 0Y100) 9.4 (9.4Y14.1) 12.5 (12.5Y15.6) ¸ MFT: S/E/F (0Y50) 9.4 (6.3Y12.5) 3.1 (3.1Y12.5) ¸ MFT: H (0Y50) 3.1 (3.1Y9.4) 6.3 (6.3Y15.6) ¸ FMS (total score, 0Y66) 5.0 (4.5Y8.5) 6.0 (5Y9) ¸ FMS: S/E/F (0Y36) 3.0 (2.5Y4.5) 2.0 (2Y2) ¸ FMS: W (0Y10) 1.0 (0Y2) 1.0 (0Y2) ¸ FMS: H (0Y14) 1.0 (0Y2) 2.0 (2Y3) ¸ FMS: C/S (0Y6) 1.0 (0.5Y1.5) 1.0 (1Y2) ¸ K-MBI 25.0 (9Y32.5) 17.0 (12Y24)
Intervention (n = 11)
Control (n = 9)
0.065 11.0 (9Y16) 9.0 (6Y11) 0.186 15.6 (9.4Y18.7) 9.4 (9.4Y12.5) 0.018 6.3 (6.3Y9.4) 3.1 (3.1Y12.5) 0.038 3.1 (3.1Y9.4) 6.3 (6.3Y12.5) 0.535 7.0 (4Y10) 7.0 (5.5Y8.5) 0.018 4.0 (2Y6) 2.0 (1.5Y2.5) 0.871 1.0 (0Y2) 2.0 (0Y2) 0.018 1.0 (0Y2) 2.0 (1.5Y3) 0.706 1.0 (0Y2) 2.0 (0.5Y2) 0.450 14.0 (10Y28) 16.0 (14.5Y21)
P 0.056 0.197 0.026 0.040 0.639 0.015 0.576 0.041 0.161 0.621
Values are given as median (interquartile range). P by Mann-Whitney U test. ¸ = posttreatment score j pretreatment score. C/S, coordination/speed; H, hand; W, wrist.
in recent studies, whether adding VR programs to conventional therapy facilitates patient progress remains to be determined.11,27 Piron et al.32 found that patients with subacute stroke who received supplemental VR therapy showed more improvements in the FMS and the Functional Independence Measure scale than did patients with subacute stroke who received only conventional therapy. The results of Piron and colleagues are therefore similar to this study’s observations. On the other hand, Crosbie et al.33 concluded that VR-based therapy had no significant effect on UE function or activity levels compared with conventional rehabilitation in patients with chronic stroke.33 By contrast, Mumford et al.34 demonstrated that VR therapy (performed for 1 hr per session for 12 sessions during the course of 4 wks) in addition to conventional physical therapy improved upper limb motor control in nine patients with traumatic brain injury. There have been several studies to clarify the effect of VR-based rehabilitation on UE function, but reported results are not consistent. On this study’s results, VR-based rehabilitation possibly demonstrates significant improvements especially in the proximal UE. This observation might stem from the authors’ selection of VR programs that mostly facilitate proximal UE recovery. The application of VR programs that instead facilitate hand movement and dexterity might considerably alter the results of this study. Conversely, the patients who received conventional OT showed more improvements in hand function. This phenomenon may be a result of fine motor training occupying one-third of the conventional OT session. For patients with proximal UE and distal UE dysfunction www.ajpmr.com
of similar degree, the addition of a VR program to conventional OT will have the advantage of improving overall UE function. The patients who received VR-based rehabilitation demonstrated improvements in K-MBI scores that were similar to the control group (21.7 [17.6] vs. 22.1 [19.5]). The authors hypothesize that the lack of superiority in the intervention group is because most of the motions in the VR programs primarily required movements of the shoulder and the elbow. Common activities of daily life require not only proximal UE movements but also fine hand movements, such as gripping objects (combs, spoons, and chopsticks) and fastening buttons. However, shoulder flexor, abductor, external rotator, internal rotator, elbow flexor, and extensor were required for activities of daily living such as washing up, combing the hair, feeding, dressing, and chair/bed transfer. The authors thought that VR-based rehabilitation can be more helpful for these muscle movements according to the S/E/F score of the FMS and the MFT. In the current study, VR therapy was conducted in the form of games, with continuous instructions and encouragement from the therapist, accompanied by various background music and ongoing visual and tactile stimulation. The authors hypothesize that these conditions offered interest, and patients can more actively participate in rehabilitation than conventional OT. The VR program also provides continuous real-time feedback regarding the patients’ performance, with their scores displayed on the television monitor or by the therapist. As demonstrated previously,35 these conditions allowed the study participants to immediately correct any errors of their motion promptly. Taken Virtual Reality–Based Rehabilitation on UE Function
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together, provision of interest, real-time feedback and task-oriented training, repetition of similar motions, as well as matching the VR intensity level with the individual’s abilities all most likely lent themselves to the recovery of UE motor function by promoting cortical reorganization. No adverse events were documented during the course of this investigation. Most of the participants in the intervention group reported that the VR tasks were easy to understand. Furthermore, the participants indicated their satisfaction with the conduct of the trial, and only two persons in the VR group stated that they did not enjoy the experience. Two patients made complaints about the composition of the programs used in the treatment session.
of the UE-FMS ranged from 4.25 to 7.25 points, depending on the different facets of UE movement with chronic stroke patients.36 The minimum clinically important difference of the MBI is 1.85 points in patients with acute stroke.37 Unlike for patients with stroke, the minimum clinically important difference of the FMS and the K-MBI has not been established for patients with brain tumor. Lastly, none of the current VR programs in the IREX System target hand movement, and the glove itself worn by the patients was recognized by a video camera during the VR training in this study, so they cannot use fingers during treatment session. Further studies considering hand function as well as the development and use of VR programs targeting hand use are required for patients with brain tumor.
Strengths and Limitations of the Study and Suggestions for Future Research
CONCLUSIONS
This is the first study designed to investigate the effect of VR-based rehabilitation combined with conventional OT for improving UE function in patients with brain tumor. The authors recruited patients with motor power in the affected arm that was higher than poor grade because patients with functional level poorer than this cannot capable of activities within the IREX System and excluded patients with recurred brain tumor, thus increasing homogeneity. The authors additionally analyzed the subsegment of the MFT and the FMS that provided more detailed information regarding UE function for each segment. However, this study has several limitations for consideration in future studies. First, this study was not a randomized controlled trial, had a small sample size, and was unable to determine the longterm effect of VR therapy. Further randomized controlled trials that include a large number of patients and long-term follow-up are thus required to fully evaluate the therapeutic potential of VR for patients with brain tumor. Second, baseline K-MBI scores were slightly lower in the intervention group than in the control group. However, there was no statistically significant difference. Third, cognitive deficits, sensory loss, and other medical issues that could influence the functional outcomes of this work were not taken into account in this study’s results. Fourth, minimum clinically important difference for each assessment used was not described in this study. Minimum clinically important difference for the BBT and the MFT has not been established in not only patients with stroke but also patients with brain tumor. Estimated clinically important difference
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The results of the current study demonstrate that VR-based rehabilitation and conventional OT are both effective treatments for the improvement in UE function in patients with brain tumor. VRbased rehabilitation combined with conventional OT may be more successful than conventional OT, especially for the restoration of proximal UE dysfunction. This effectiveness may be applied similarly to patients with benign and malignant tumor. In addition to its ample feasibility for application to patients with brain tumor, VR therapy is safe, well tolerated, and helpful for functional UE recovery in patients with brain tumor.
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