To evaluate the effectiveness of intensive rehabilitation to support recovery of neurological function after brain tumor surgery and assess long-term satisfaction.
This retrospective study included patients with neurological impairment after brain tumor surgery who underwent intensive rehabilitation therapy between December 2013 and May 2017. To assess effectiveness of rehabilitation, functional outcomes (motor, cognition, and activities of daily living [ADL]) were compared between brain tumor group and a control group enrolling stroke patients who received equivalent rehabilitation during the study period. Long-term satisfaction with rehabilitation was evaluated by surveying family caregivers.
This study included 21 patients with benign brain tumor, 14 with malignant brain tumor, and 108 with stroke. Significant and similar improvement in motor, cognition, and ADL function were noted in both the brain tumor group and the stroke group. Malignancy status did not influence the extent of functional improvement. According to medical records and surveys, 9 (69.2%) patients with malignant tumor and 2 (11.8%) with benign tumor had expired by the time of the survey. Most family caregivers confirmed that rehabilitation was effective for functional improvement (>60%), expressing overall satisfaction and stating they would recommend such therapy to patients with similar conditions (approximately 70%).
Intensive rehabilitation may help promote functional improvement following brain tumor surgery regardless of malignancy compared with stroke patients. Family caregivers expressed overall satisfaction with rehabilitation at long-term follow-up. These findings support the provision of intensive rehabilitation therapy for neurologic function recovery following brain tumor surgery.
Brain tumor is a major cause of disability. The prevalence of intracranial tumors is increasing [
In 1978, Lehmann et al. [
While the short-term effectiveness of rehabilitation therapy in brain tumor patients has been recognized, it remains controversial whether rehabilitation is meaningful and necessary if the survival rate is low and the recurrence rate is high. So far, no studies have addressed this important question. In the absence of an objective indicator of the potential need and benefit of rehabilitation for patients with brain tumors, long-term satisfaction of family caregivers may serve as a surrogate measure in the context of evolution of neurologic function throughout patients’ remaining life.
In this study, we aimed to (1) comparatively assess the effectiveness of intensive rehabilitation therapy for improving neurological deficit following brain tumor surgery, taking functional outcomes of rehabilitation in stroke patients as reference as the usefulness of intensive rehabilitation in stroke patients has already been validated [
This study was approved by the Institutional Review Board of CHA Bundang Medical Center (No. 2018-01-002-001). We retrospectively reviewed medical records maintained at a single university hospital rehabilitation center and identified patients with neurological impairment after brain tumor resection surgery or stroke who were admitted for intensive rehabilitation between December 2013 and May 2017.
To minimize bias, all patients fulfilling the inclusion/exclusion criteria during the study period were enrolled in this study. Inclusion criteria were (1) brain tumor or stroke defined as brain lesions on computed tomography or magnetic resonance imaging; (2) admission for rehabilitation within <4 months since brain tumor resection surgery or stroke onset; (3) age >18 years; and (4) discharged for >1 year. Exclusion criteria were (1) combined neurodegenerative disease; and (2) persistent minimally conscious state or vegetative status. Patients with brain tumor were divided into subgroups based on malignancy status (benign and malignant) defined according to the World Health Organization classification [
The rehabilitation center implements a routine process for baseline functional assessment soon after admission and follow-up assessment at >1 month after admission. Standard rehabilitation therapy consisted of 1 hour of physical therapy and 1 hour of occupational therapy, with sessions conducted 5 days/week during hospitalization. The aim of rehabilitation therapy in patients with neurological deficit was to facilitate their self-management ability. The rehabilitation protocol was developed by the clinical therapy team.
Physical therapy focused on range-of-motion exercise, progressive resistive exercise, balance training, endurance training, and gait training. Occupational therapy focused on cognitive ability enhancement, upper extremity proprioceptive neuromuscular facilitation, and activities of daily living (ADL) training. Outcome analysis was conducted based on the rehabilitation center’s records documenting results of baseline assessment conducted within 5 days of admission and results of follow-up assessment. Functional assessments was conducted using the following tools: Fugl-Meyer Assessment (FMA) index, Berg Balance Scale (BBS) score, Korean version of the Modified Barthel Index (K-MBI) score, Korean Mini-Mental State Examination (K-MMSE) score, and intelligence quotient (IQ) score on the Korean version of the Wechsler Adults Intelligence Scale. Among brain tumor patients, the Eastern Cooperative Oncology Group (ECOG) score was also evaluated to confirm the functional level. In our rehabilitation center, reliability tests for these above-mentioned scores are performed regularly, with all intraclass correlation coefficients for inter-rater reliability maintained at >0.9. Demographic and clinical characteristics of patients were obtained from medical records. For patients with brain tumors, additional information was collected, including histologic type, location of the tumor, recurrence status (primary or recurred tumor), and duration of surgery.
Long-term satisfaction with rehabilitation therapy was assessed via telephone survey of family caregivers of patients with brain tumors. The survey was conducted after May 2018, when more than 1 year had passed since the discharge of the last patient enrolled in this study. The survey contained six items that evaluated the opinion of caregivers on whether rehabilitation brought improvement in (1) motor function, (2) cognition, (3) ADL; (4) whether the intensity of rehabilitation therapy was adequate; (5) their overall satisfaction with rehabilitation; and (6) whether they would recommend such rehabilitation to other patients with similar conditions (
The usefulness of rehabilitation therapy has already been validated in stroke patients [
The Statistical Package for the Social Sciences (SPSS) version 21.0 for Windows (IBM, Armonk, NY, USA) was used for all data analyses. Independent t-test and chisquare test were used to compare brain tumor and stroke groups of patients in terms of demographic and baseline characteristics. The significance of functional improvements in each group was confirmed using the Wilcoxon signed-rank test which was applied for each outcome parameter. Mann-Whitney U test was used to compare outcomes of rehabilitation between brain tumor and stroke groups as well as between benign and malignant tumor subgroups. In addition to effectiveness of rehabilitation for each outcome parameter, the efficiency of rehabilitation was calculated as the amount of change divided by the length of rehabilitation. It represents the average degree of improvement that can be achieved daily through rehabilitation therapy. Multivariate linear regression analysis was used to identify baseline predictors of rehabilitation outcome in brain tumor patients. The survival rate of the brain tumor group was analyzed using the Kaplan-Meier survival curve. Chi-square test was performed to detect associations of overall satisfaction with other variables such as long-term improvements in motor, cognition, and ADL function; long-term survival status; and malignancy status on pathology examination. Statistical significance was set at p<0.05.
Of 35 brain tumor patients included in this study, 21 had benign tumor and 14 had malignant tumor. As controls, we enrolled 108 patients with stroke (
There were no significant differences in ECOG score, tumor location, or lesion size between benign and malignant tumor subgroups (
Significant improvement in FMA, BBS, K-MBI, KMMSE, and IQ scores were noted within both brain tumor and stroke groups (each p<0.001) (
Among brain tumor patients, the improvement in ECOG score was not significantly affected by malignancy status (
Chart review and telephone survey revealed that 2 of 17 patients (11.8%) with benign tumor had expired by the time of the survey, with a mean survival period of 116.6 months since surgery and 112.6 months since initiation of rehabilitation therapy (
Twenty-six family caregivers of patients with brain tumors (benign, n=17; malignant, n=9) responded to the telephone survey which was conducted at an average of 2.23 years after patient discharge. Among 26 respondents, family caregivers of 19 survivors (benign tumor, n=15; malignant tumor, n=4) provided information regarding the long-term functional status (
Most family caregivers felt that rehabilitation was effective for each functional domain evaluated (motor function, 65.4%; cognition, 61.6%; ADL function, 61.6%) (
Approximately 77% of family caregivers were satisfied with the intensity of rehabilitation therapy, 73.1% expressed overall satisfaction with the rehabilitation therapy, and 69.2% stated they would recommend such rehabilitation therapy to patients in a similar situation (
On chi-square test, long-term satisfaction expressed by family caregivers showed significant association with current motor function (p=0.046), but not with current cognitive function (p=0.069), ADL function (p=0.314), survival status (p=0.300), or malignancy status (p=0.107).
In this study, we found that brain tumor patients who received intensive rehabilitation for motor, balance, cognition, and ADL function exhibited significant functional improvement. This improvement was similar to that achieved in patients with stroke. It was not affected by malignancy status. Furthermore, our survey of family caregivers conducted at 1–4 years after intensive rehabilitation suggested that brain tumor survivors had relatively well-maintained status of motor, cognition, and ADL function. Moreover, caregivers of brain tumor patients expressed high rates of long-term satisfaction with the intensive rehabilitation therapy. Despite the relatively high percentage of patients with malignant brain tumors or who died, their satisfaction with the rehabilitation therapy remained high.
The demand for intensive rehabilitation therapy is steadily increasing as treatment options advance. However, intensive rehabilitation therapy appears to be underused in brain tumor patients, especially if the tumor is malignant [
Sherer et al. [
Previous studies on the independence of stroke patients employing the Barthel Index and the Functional Independence Measure have reported that poor functional state at admission is associated with poor functional improvement [
In this study, we surveyed long-term satisfaction of family caregivers as a surrogate of the long-term evolution of patients’ neurological function in order to determine whether rehabilitation could provide meaningful long-term benefits beyond functional improvement achieved in the early period. Several studies have reported the satisfaction with rehabilitation therapy and longterm outcomes among stroke patients [
The satisfaction level expressed by family caregivers with respect to rehabilitation therapy was significantly associated with current motor function, but not with survival status or malignancy status. Among functional domains, motor ability is a significant predictor of functional independence in stroke patients [
This study has several limitations. First, the size of the brain tumor group was smaller than the minimum sample size estimated based on power analysis. Therefore, our investigation is considered a pilot study and findings warrant validation in larger patient populations. Furthermore, we could not perform further analysis of outcomes and satisfaction stratified according to histological type, lesion site, tumor size, or treatment strategy (tumor resection, radiotherapy, and chemotherapy). Second, long-term outcome was determined only by subjective judgment of family caregivers. Although a quantitative assessment of the current functional status would be more appropriate from a purely methodological perspective, the questionnaire-based survey of family caregivers was more appropriate from a practical perspective as some patients died or could not have traveled to the hospital. Third, as the telephone survey was conducted at 1–4 years post-discharge, these data might have been affected by recall bias. Moreover, certain important aspects (such as whether or not patients received additional rehabilitation therapy) were not covered by the survey. Fourth, this study did not include a true control group (i.e., patients who did not receive rehabilitation therapy after brain tumor surgery). Thus, we could not confirm whether the improvement in neurological function was due to natural recovery or rehabilitation.
To conclude, brain tumor patients who received intensive rehabilitation following surgery achieved improvements in the outcomes of motor, cognition, and ADL function similar to those noted in stroke patients, regardless of malignancy status. Moreover, despite the low survival rate and high recurrence rate in patients with malignant brain tumors, their family caregivers expressed a high degree of satisfaction with functional improvements following intensive rehabilitation therapy. These findings suggest that postoperative rehabilitation should be considered for patients with brain tumors regardless of tumor pathology as such therapy may be beneficial, despite such patients have a low survival rate.
No potential conflict of interest relevant to this article was reported.
This research was supported by a grant (No. HI16C1559) of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) funded by the Ministry of Health & Welfare, Republic of Korea.
Conceptualization: Kim M, Cho KG. Methodology: Yu J, Jung Y, Park J. Formal analysis: Kim JM, Suh M. Writing – original draft: Kim M. Writing – review and editing: Kim M. Approval of final manuscript: all authors.
Supplementary materials can be found via
Telephone survey questionnaire for satisfaction on intensive rehabilitation therapy
Recruitment flowchart detailing the number of participants included and excluded. WHO, World Health Organization.
Comparison of rehabilitation outcome for (A) efficiencies in brain tumor and stroke groups, and (B) efficiencies in malignant and benign brain tumor groups. There is no significant difference when efficiencies between two groups (brain tumor vs. stroke and malignant vs. benign brain tumor) are compared by Mann-Whitney U test. The bold line in the box represents the median value. The interquartile range box represents the middle 50% of each data. The whisker represents ranges for the bottom 25% and the top 25%, excluding outliers. FMA, Fugl-Meyer Assessment; BBS, Berg Balance Scale; K-MBI, Korean version of Modified Barthel Index; K-MMSE, Korean Mini-Mental State Examination; IQ, intelligence quotient.
Survival estimates in patients with brain tumor. The survival rate was analyzed using the Kaplan-Meier survival curve. Cumulative survival probability is drawn according to different pathology (benign vs. malignant) in brain tumor since brain tumor operation (A) and initiation of rehabilitation therapy (B). (A) Since brain tumor operation, overall mean survival was 93.6 months. It was 116.6 months and 52.9 months for benign and malignant tumors, respectively. (B) Since initiation of rehabilitation therapy, overall mean survival was 89.3 months. It was 112.6 months and 48.4 months for benign and malignant tumors, respectively.
Results of telephone survey about current functions in patients with brain tumor. Opinion of family caregivers on current status of motor, activities of daily living (ADL), and cognitive function compared to the status on discharge in survived patients (3-point scale: improved, similar, and worsened) in benign brain tumor patients (n=15) (A) and malignant brain tumor patients (n=4) (B).
Results of telephone survey about satisfaction in patients with brain tumor. (A) Brain tumor patients in total (n=26), (B) patients with malignant brain tumor (n=9), and (C) deceased patients with both benign and malignant brain tumor (n=7) are depicted.
Demographic and disease-related characteristics
Brain tumor group (n=35) | Stroke group (n=108) | p-value | |
---|---|---|---|
Age (yr) | 57.6±13.2 | 60.9±11.6 | 0.275 |
Gender | 0.890 | ||
Male | 18 (51.4) | 57 (52.8) | |
Female | 17 (48.6) | 51 (47.2) | |
Lesion location | 0.527 | ||
Right hemisphere | 16 (45.7) | 47 (43.5) | |
Left hemisphere | 14 (40.0) | 41 (38.0) | |
Cerebellum | 2 (5.7) | 9 (8.3) | |
Brain stem | 3 (8.6) | 11(10.2) | |
Tumor etiology (WHO grade) | |||
I (benign tumor) | 11 (31.4) | NA | - |
II (benign tumor) | 10 (28.6) | ||
III (malignant tumor) | 4 (11.4) | ||
IV (malignant tumor) | 10 (28.6) | ||
Recurrence | |||
Primary | 24 (31.4) | ||
Recurrent | 11 (68.6) | ||
Length of rehabilitation (day) | 37.2±11.9 | 36.4±6.7 | 0.759 |
Values are presented as number or mean±standard deviation or number of patients (%).
Mean value and the percentage of each groups were compared by independent t-test.
Continuous data were tested by independent t-test and categorical data were tested by chi-square test.
WHO, World Health Organization; NA, not applicable.
Brain tumor characteristics
Benign brain tumor (n=21) | Malignant brain tumor (n=14) | p-value | |
---|---|---|---|
Lesion location | 0.537 | ||
Right frontal | 4 (19.0) | 3 (21.4) | |
Right temporal | 2 (9.5) | 2 (14.3) | |
Right parietal | 0 (0) | 1 (7.1) | |
Right hypothalamus | 1 (4.8) | 0 (0) | |
Right thalamus | 0 (0.0) | 1 (7.1) | |
Left frontal | 1 (4.8) | 1 (7.1) | |
Left temporal | 4 (19.0) | 2 (14.3) | |
Left parietal | 1 (4.8) | 1 (7.1) | |
Left thalamus | 0 (0) | 1 (7.1) | |
Left cingulate gyrus | 0 (0) | 1 (7.1) | |
Left lateral ventricle | 3 (14.3) | 0 (0.0) | |
Cerebellum | 1 (4.8) | 1 (7.1) | |
Brain stem | 3 (14.3) | 0 (0) | |
Skull base | 1 (4.8) | 0 (0) | |
Lesion size, long axis (cm) | 0.537 | ||
2–3 | 3(14.3) | 2 (14.3) | |
3–4 | 7 (33.3) | 4 (28.6) | |
4–5 | 6 (28.6) | 2 (14.3) | |
5–6 | 4 (19.0) | 3 (21.4) | |
6–7 | 1 (4.8) | 3 (21.4) | |
Treatment modality | <0.001 |
||
Surgery | 13 (61.9) | 0 (0) | |
Surgery+chemotherapy | 1 (4.8) | 2 (14.3) | |
Surgery+radiotherapy | 7 (33.3) | 4 (28.6) | |
Surgery+chemotherapy+radiotherapy | 0 (0) | 8 (57.1) | |
Recurrence | |||
Primary | 16 (76.2) | 8 (57.1) | <0.001 |
Recurrent | 5 (23.8) | 6 (42.9) | |
Initial ECOG scale | |||
1 | 2 (9.5) | 0 (0) | 0.071 |
2 | 4 (19.0) | 3 (14.3) | |
3 | 7 (33.3) | 9 (42.9) | |
4 | 8 (38.1) | 2 (9.5) |
Values are presented as number of patients (%).
Benign brain tumor subgroup included atypical meningioma, atypical neurocytoma, chordoid glioma, chordoma, craniopharyngioma, hemangioblastoma, meningothelial meningioma, pilocytic astrocytoma, pleomorphic xanthoastrocytoma, reactive gliosis and schwannoma. Malignant brain tumor subgroup included anaplastic astrocytoma and glioblastoma.
ECOG, Eastern Cooperative Oncology Group.
p<0.001, when continuous data were tested by independent t-test, and categorical data were tested by chi-square test.
Rehabilitation outcomes for brain tumor and stroke groups
Brain tumor group (n=35) |
Stroke group (n=108) |
p-value |
|||||
---|---|---|---|---|---|---|---|
Baseline | Discharge | p-value (within groups) | Baseline | Discharge | p-value (within groups) | ||
FMA score | 34.5±22.2 | 49.1±17.5 | <0.001 |
30.1±21.6 | 41.8±21.0 | <0.001 |
0.737 |
BBS score | 17.0±15.9 | 35.6±17.7 | <0.001 |
20.7±18.0 | 35.2±17.7 | <0.001 |
0.929 |
K-MBI score | 36.9±18.5 | 58.3±20.1 | <0.001 |
38.6±21.0 | 56.7±23.2 | <0.001 |
0.447 |
K-MMSE score | 17.3±10.1 | 23.1±7.6 | <0.001 |
16.7±8.2 | 21.1±7.1 | <0.001 |
0.569 |
IQ score | 67.1±18.1 | 78.9±14.8 | <0.001 |
69.6±18.4 | 78.5±18.4 | <0.001 |
0.180 |
Values are presented as mean±standard deviation.
FMA, Fugl-Meyer Assessment; BBS, Berg Balance Scale; K-MBI, Korean version of Modified Barthel Index; K-MMSE, Korean Mini-Mental State Examination; IQ, intelligence quotient.
Compared difference of each score (score at discharge – score at admission) between two groups (brain tumor vs. stroke) by Mann-Whitney U test.
p<0.001 when comparing each scores of baseline and discharge within same group by Wilcoxon-signed rank test.
Rehabilitation outcomes for benign and malignant brain tumor subgroups
Benign brain tumor (n=21) |
Malignant brain tumor (n=14) |
p-value |
|||||
---|---|---|---|---|---|---|---|
Baseline | Discharge | p-value (within groups) | Baseline | Discharge | p-value (within groups) | ||
FMA score | 36.7±22.3 | 51.1±15.4 | <0.001 |
31.1±20.8 | 45.9±20.7 | 0.002 |
0.434 |
BBS score | 19.1±17.1 | 38.0±15.7 | <0.001 |
13.9±13.0 | 32.1±20.1 | 0.002 |
0.210 |
K-MBI score | 37.7±20.2 | 61.4±21.6 | <0.001 |
35.9±15.6 | 53.8±18.4 | 0.016 |
0.702 |
K-MMSE score | 15.5±7.3 | 23.5±5.1 | <0.001 |
19.3±9.8 | 22.6±7.1 | <0.001 |
0.220 |
IQ score | 63.9±16.1 | 79.1±12.8 | 0.001 |
71.5±20.7 | 78.5±17.7 | 0.002 |
0.156 |
ECOG scale | 3.0±0.8 | 2.9±0.4 | <0.001 |
1.86±0.7 | 2.1±0.7 | 0.011 |
0.175 |
Values are presented as mean±standard deviation.
FMA, Fugl-Meyer Assessment; BBS, Berg Balance Scale; K-MBI, Korean version of Modified Barthel Index; K-MMSE, Korean Mini-Mental State Examination; IQ, intelligence quotient; ECOG, Eastern Cooperative Oncology Group.
Compared difference of each score (score at discharge – score at admission) between two groups (brain tumor vs. stroke) by Mann-Whitney U test.
p<0.05,
p<0.01,
p<0.001 when comparing each scores of baseline and discharge within same group by Wilcoxonsigned rank test.
Multivariate linear regression analysis between initial state and rehabilitation outcomes in brain tumor patients
Variable | Outcome | Predictor | Adjusted R2 | p-value |
---|---|---|---|---|
Brain tumor group | Change of FMA | Baseline FMA | 0.032 | <0.001 |
Change of BBS | Baseline BBS | 0.084 | 0.041 |
|
Change of MBI | Baseline K-MBI | 0.354 | 0.034 |
|
Change of K-MMSE | Baseline K-MMSE | 0.354 | <0.001 |
|
Baseline IQ | 0.200 | 0.004 |
||
Change of IQ | Baseline K-MMSE | 0.181 | 0.006 |
|
Baseline IQ | 0.402 | <0.001 |
||
Benign tumor subgroup | Change of FMA | Baseline K-MMSE | 0.263 | 0.010 |
Baseline IQ | 0.456 | <0.001 |
||
Change of BBS | Baseline BBS | 0.150 | 0.047 |
|
Change of K-MBI | Baseline K-MBI | 0.219 | 0.019 |
|
Change of K-MMSE | Baseline K-MMSE | 0.918 | 0.005 |
|
Baseline IQ | 0.294 | 0.007 |
||
Change of IQ | Baseline K-MBI | 0.344 | 0.003 |
|
Malignant tumor subgroup | Change of BBS | Baseline FMA | 0.252 | 0.039 |
Change of K-MBI | Baseline K-MBI | 0.185 | 0.029 |
|
Change of K-MMSE | Baseline K-MBI | 0.373 | 0.012 |
|
Baseline K-MMSE | 0.337 | 0.017 |
||
Change of IQ | Baseline IQ | 0.256 | 0.038 |
FMA, Fugl-Meyer Assessment; BBS, Berg Balance Scale; K-MBI, Korean version of Modified Barthel Index; K-MMSE, Korean Mini-Mental State Examination; IQ, intelligence quotient.
p<0.05,
p<0.01,
p<0.001 when comparing each score of baselines and change within the same group by multivariate linear regression analysis.