Authors: Paulo Bazile da Silva, MSc Fabiane Nunes Antunes, PT Patrı´cia Graef, MSc Fernanda Cechetti, PhD Aline de Souza Pagnussat, PhD
Affiliations:
Stroke
ORIGINAL RESEARCH ARTICLE
From the Programa de Po´s-graduac¸a˜o em Cieˆncias da Reabilitac¸a˜o (PBdS, FNA, FC, ASP), Departamento de Fisioterapia (PG, FC, ASP), and Programa de Po´s Graduac¸a˜o em Cieˆncias da Sau´de (ASP), Universidade Federal de Cieˆncias da Sau´de de Porto Alegre, Porto Alegre, Rio Grande do Sul, Brazil.
Correspondence: All correspondence and requests for reprints should be addressed to: Aline de Souza Pagnussat, PhD, Departamento de Fisioterapia, Universidade Federal de Cieˆncias da Sau´de de Porto Alegre, Rua Sarmento Leite, 245, 90050-170, Porto Alegre, RS, Brazil.
Disclosures: Supported by grants from the Brazilian agencies CNPq (National Council of Technological and Scientific, Brazil) and the National Council for the Improvement of Higher Education (CAPES-Brazil). 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.
0894-9115/15/9401-0011 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000135
Strength Training Associated with Task-Oriented Training to Enhance Upper-Limb Motor Function in Elderly Patients with Mild Impairment After Stroke A Randomized Controlled Trial ABSTRACT da Silva PB, Antunes FN, Graef P, Cechetti F, Pagnussat AS: Strength training associated with task-oriented training to enhance upper-limb motor function in elderly patients with mild impairment after stroke: a randomized controlled trial. Am J Phys Med Rehabil 2015;94:11Y19.
Objective: The aim of this study was to verify the effects of loaded exercises associated with a task-oriented training (TOT) program in the recovery of upperlimb function in individuals with chronic hemiparesis after stroke. Design: This study used a single-blinded, randomized controlled trial. Patients were included into two TOT groups: one that performed the task-oriented therapy without load (TOT group, n = 10) and another one that performed task-oriented therapy with personalized resistance (TOT_ST group, n = 10) for 6 wks, for a total of 12 sessions. Main measures included The Upper Extremity Performance Test, shoulder flexor and handgrip strength, shoulder active range of motion, motor impairment (Fugl-Meyer Scale), and muscle tone.
Results: The TOT_ST group demonstrated better scores relating to unilateral tasks and in the quality aspects of bilateral movements (The Upper Extremity Performance Test, P = 0.04) at the end of rehabilitation protocol. The highest muscle force gain was reached by the TOT_ST group for the shoulder flexors (P = 0.001). Similarly, the active range of motion (P = 0.01) and Fugl-Meyer scores (P = 0.001) were higher in the TOT_ST group compared with the TOT group. Both groups showed improvement after training.
Conclusions: Strength training was able to intensify the upper-limb rehabilitation, as demonstrated by the superior scores achieved by the TOT_ST group in most of the evaluated parameters. Muscle strength training might be a pivotal element of the task-oriented rehabilitation program of chronic patients with mild impairment after stroke. Key Words:
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Chronic Hemiparesis, Physiotherapy, Rehabilitation, Muscle Weakness
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C
hronic diseases are the major cause of death and disability worldwide. Among these disorders, stroke is the leading cause of long-term physical impairment. The most prominent motor deficit after stroke is paresis of the side of the body contralateral to the cerebrovascular event, which can permanently affect arm-hand performance.1 Contemporary research has demonstrated weakness as one of the most important primary impairments in persons after stroke. Weakness has been shown to compromise many meaningful daily tasks and greatly affects participation and qualityof-life of individuals with hemiparesis.2Y5 Weakness has been reported as decreased torque generation at the elbow,6 shoulder,7 fingers, and thumb,5,8,9 which can be a consequence of an abnormal motor activation and/or physical inactivity. A disabling stroke combined with a sedentary lifestyle accelerates the gradual loss of muscle mass and magnifies the usual age-associated loss of fat-free mass, which consequently leads to functional deficits.10 The decrease in muscle strength can occur as a consequence of structural and functional changes in spastic muscles. These modifications include altered muscle fiber size, fiber type distribution, proliferation of extracellular matrix material, increased stiffness of spastic muscle cells, and inferior mechanical properties of extracellular content.11,12 In the chronic phase after a stroke, strengthening interventions can maximize the capacity for voluntary neuromuscular activation. This increased muscle strength might be able to promote functional improvement and potentially improve quality-of-life without negative adverse effects (such as the increase of hypertonia and pain).4,13,14 Accordingly, methods consisting of strength and endurance training are now part of the programs regularly offered to patients after stroke.15 There are several research studies that document the effectiveness of task-oriented training (TOT) as a neurologic treatment approach.16Y18 An ideal task-oriented protocol should be composed of unilateral and bilateral activities geared toward a clear functional goal (similar to activities of daily living using real-life objects) and performed in a contextspecific environment.19 Although the resistance training could be an effective training method to improve and maintain muscle strength in the short term and long term during stroke rehabilitation,14 a patient-customized training load is not always a part of the task-oriented rehabilitation program. Several studies using TOT protocols have been conducted without specifically including strength training.19
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Considering that post-stroke patients are likely to benefit from rehabilitation interventions that maximize the capacity for voluntary neuromuscular activation, the aim of this study was to determine the effectiveness of a patient-customized training load as part of the task-oriented upper-limb rehabilitation program in individuals with chronic hemiparesis and mild impairment after stroke. It was hypothesized that muscle strength training could be a pivotal element of the task-oriented rehabilitation program. Strength training might be more effective in improving muscle strength, motor skills, and functional recovery during short-term stroke rehabilitation.
METHODS Participants This prospective, randomized controlled trial was registered and allocated by the Brazilian Clinical Trials Registry and included concealed randomization and blinded assessments. In all, 218 adults with chronic hemiparesis were screened, and 20 of them were recruited from two medical centers during 18 mos (Fig. 1). Participants provided informed written consent to a protocol approved by the Universidade Federal de Cieˆncias da Sau´de de Porto Alegre’s Human Research Ethics Committee (protocol number 11-826). The inclusion criteria were (1) time since the onset of a single, unilateral stroke ranging between 6 mos and 5 yrs (chronic stage); (2) ability to comprehend simple instructions (Mini-Mental State Examination with a minimum score of 20); (3) no pain, contractures, or severe weakness in the shoulder muscles (G3 in the Manual Muscular Testing or lack of ability to perform 60 degrees of active shoulder range of motion [ROM] against the gravity); and (4) not submitted to other upper-limb rehabilitation programs during the participation in this study. Participants were excluded if they had (1) other neurologic, neuromuscular, or orthopedic disease; (2) severe comorbidities; or (3) severe spasticity of the elbow flexors that compromised the task performance (93 points according to the Modified Ashworth Scale).
Study Design During the 6-wk intervention period, patients were included in a rehabilitation protocol composed by task-oriented activity with or without strength training. Patients were stratified based on the strength of glenohumeral forward flexion, which was quantified with a load cell (Miotec, Brazil). The allocation schedule was generated and concealed in sequentially numbered, sealed, opaque envelopes. Random assignment was computer-generated by a physiotherapist
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FIGURE 1 Subject recruitment and attrition flowchart. who was not involved in the patient selection. Participants were randomly assigned to two intervention groupsVtask-oriented without strength training (TOT, n = 10) or task-oriented with strength training (TOT_ST, n = 10)V1 wk before the start of the intervention. Baseline evaluation and postintervention measures were performed by a well-trained research assistant blind to group allocation. Participants received a 30-min, therapist-supervised, home rehabilitation program two times per week for 6 wks (total of 12 sessions). Each session began with a period of slow-sustained stretching and passive ROM of the hemiparetic upper limb, focusing on the tone normalization of the elbow and wrist flexors and shoulder abductors. Rehabilitation exercises were performed with subjects seated in a chair, which allowed for a posture in which the knees and hips were maintained at 90 degrees. A belt was used to restrain the trunk and avoid compensatory movements.20 The load determination for the strength protocol was based on the ability to generate maximal force during www.ajpmr.com
glenohumeral forward flexion on the hemiparetic side. The load used for training remained at 60% of the maximum value during the entire rehabilitation period.
Intervention The rehabilitation protocol consisted of five taskoriented movements chosen to meet the following criteria: unilateral (only the paretic limb) and bilateral functional exercises (both upper limbs used to perform the task), activity-of-daily-living goal, contextspecific environment using real-life object manipulation, and exercised in multiple movement planes. Rehabilitation exercises simulated the following activities of daily living: brushing hair, putting on a scarf, feeding, handling a coffee pot, and putting a pot on a high cabinet shelf. All activities were performed with increasing difficulty levels (progression in ROM according to the patient capacity), followed with feedback of the exercise performance, and reinforced by verbal instructions. Strength Training in Elderly Patients Post-Stroke
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Both groups received the same number and frequency of sessions, which consisted of ten repetitions of the same movement with a 3-min resting period between each movement. The TOT and TOT_ST groups randomly performed all of the five tasks each day. Patients from the TOT_ST group performed all tasks with load resistance (60% of the maximum baseline force) put on the arm as a bracelet or into a jug. Both groups’ rehabilitation was performed at home. The execution of the exercises was always supervised by a physiotherapist. Two physiotherapists conducted the rehabilitation protocol for patients from both groups. Therapists received training by the same instructor and used similar verbal cues for patients in both groups.
Outcome Measures The primary clinical outcome measure for improving upper-limb performance in unilateral and bilateral activities was the Test d’Evaluatio´n des Membres Superieus des Personnes Age´es (TEMPA).21 This test was used to evaluate the performance of the upper limb in the completion of functional activities. The Brazilian version of the TEMPA is a protocol for the observation of upper-limb performance composed of eight standardized tasks (four bilateral and four unilateral ones), which represent daily activities. Each task was evaluated by three criteria: speed of execution, functional levels or functional graduation, and analyses of the performed tasks. The functional level or functional graduation refers to the individual’s autonomy in each task measured on a four-level scale as follows: tasks (0) were successfully completed without hesitation or difficulty; (j1) were completed, but with some difficulty; (j2) were partially executed or some steps were performed with significant difficulty; and (j3) failed to be completed, even if any degree of assistance was offered. The analyses of the performed tasks quantified the difficulties experienced by the subjects according to five dimensions related to upper-extremity sensory motor
skills: strength, ROM, precision of gross movements, prehension, and precision of fine movements. The total scores were determined by adding the scores obtained from both the unilateral and bilateral tasks. The higher score represents the best performance, ranging from 0 to j150. Adequate reliability has been reported using the TEMPA scale for adults with hemiparesis.21 Secondary outcome measures included shoulder and grip strength (in kilograms and pounds, respectively), active shoulder ROM (degrees), motor recovery of the upper limbs, and muscle tone. Three grip and shoulder strength measures were taken using the Jamar hydraulic hand dynamometer (Sammons Preston Corp) and load cell (Miotec, Brazil), respectively, with standardized positioning and instruction. The highest score of the three trials was retained. Standard goniometry was used to measure active glenohumeral forward flexion ROM. Motor recovery of the upper limbs was evaluated using the upperextremity session of the Fugl-Meyer assessment scale. The Fugl-Meyer Scale includes four motor subitems relevant to the involved upper extremity: (1) shoulder/ elbow/forearm, (2) wrist, (3) hand, and (4) speed coordination. Each item was rated on a 3-point scale (0, cannot perform; 1, partially performed; 2, fully performed) for a 66-point maximum. The Modified Ashworth Scale22 was used to evaluate the elbow flexors’ muscle tone.
Statistical Analysis The sample size was determined to detect group differences of 3 points in the primary clinical outcome scale (TEMPA, unilateral task analysis subsection), with a power of 70% for a two-tailed t test with significance set at a level of 0.05.23 Results are presented as median (minimum/maximum) or mean (SD). Data normality was tested using the ShapiroWilk test, and the homogeneity of variance was tested by Levene statistic. The Mann-Whitney U test and independent samples t test were used for nonparametric
TABLE 1 Characteristics of the participants
Sex, n (%) Male Female Paretic side, n (%) Right Left Age, mean (SD), yrs Time since onset, mean (SD), mos a
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TOT, n = 10
TOT_ST, n = 10
4 (40) 6 (60)
3 (30) 7 (70)
3 (30) 7 (70) 70.4 (7.83) 41.4 (11.89)
2 (20) 8 (80) 70.3 (7.83) 40.2 (13.48)
Pa
1.000 1.000 t = 0.03, P = 0.978 t = 0.2, P = 0.835
Fisher’s exact test for proportions. t test for continuous variables.
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Strength Training in Elderly Patients Post-Stroke
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15
Pretest
Posttest
j15 (j48/j9), j9.0 (j44.0/0), [j33.0 to j7.0] [j32.4 to j4.5] j14 (j22/0), j4.5 (j17/0), [j16.0 to j2.7] [j13.3 to j1.0] j21.5 (j60/j12), j12.5 (j55/0), [j41.4 to j7.5] [j23.2 to j40.7] j19.0 (j27/0), j4.5 (j19/0), [j19.3 to j2.4] [j16.8 to j0.9] j39.0 (j84/j10), j16.0 (j72/0), [j60.4 to j13.0] [j56.4 to j8.7]
Z = j2.54, P = 0.011 Z = j2.54, P = 0.011 Z = j2.54, P = 0.011 Z = j2.53, P = 0.012 Z = j2.66, P = 0.008
j1.0 (j11/0), [j5.4 to j0.5] 0 (j3/0), [j3.5 to 0.1]
Posttest
j4.5 (j12/j3), [j7.9 to j3.6] j4.0 (j6/0), [j3.4 to 0.4]
Pretest
TOT_ST, n = 10
Z = j2.27, P = 0.023 Z = 2.23, P = 0.025
Pa
Scores
Z = j2.67, P = 0.008 Z = j2.52, P = 0.012 Z = j2.81, P = 0.005 Z = j2.53, P = 0.011 Z = j2.81, P = 0.005
Z = j2.53, P = 0.012 Z = j2.56, P = 0.011
Pa
42 31 42 41 45
25 13 28 17
73
29 8
71
Post-Pre, % 15
Post-Pre, %
TOT, n = 10 TOT_ST, n = 10
Change Scores, %
Values are presented as median (min/max), [95% confidence interval]. Wilcoxon’s and Mann-Whitney U tests were used for intragroup and intergroup comparisons, respectively. a Within-group comparison. b Between-group comparison.
Functional Graduate Unilateral tasks j4.0 (j12/0), j3.0 (j12/0), [j8.2 to j2.1] [j7.1 to j1.2] Bilateral tasks j2.0 (j9/0), j1.0 (j6/0), [j2.0 to 0.06] [j0.9 to 0.1] Task Analysis Unilateral tasks j15.5 (j48/0), j12.0 (j48/0), [j25.7 to j5.0] [j23.3 to j2.2] Bilateral tasks j8.0 (j40/0), j5.5 (j34/0), [j13.1 to j1.8] [j11.5 to 0.1] Unilateral j19.5 (j60/0), j15.0 (j60/0), total score [j32.6 to j6.7] [j29.9 to j3.0] Bilateral j10.0 (j49/0), j6.0 (j40/0), total score [j15.1 to j1.8] [j12.4 to 0.2] j27.0 (j109/j105), j21.5 (j92/j1), Unilateral and [j47.3 to j9.6] [j41.9 to j3.2] bilateral tasks’ scores combined
TEMPA
TOT, n = 10
TABLE 2 Clinical primary measurements
U = 27.0, P = 0.082 U = 44.0, P = 0.648 U = 23.0, P = 0.041 U = 41.0, P = 0.490 U = 32.5, P = 0.186
U = 31.5, P = 0.156 U = 24.5, P = 0.049
Pb
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t = j3.70, P = 0.004 t = 4.86, P = 0.001 t = j5.06, P = 0.001 t = j2.38, P = 0.041 Z = 0.00, P = 1.0
1.0 (0/3.0), [0.2Y1.6]
P
3.6 (1.4), [2.6Y4.6] 17.6 (6.9), [12.6Y22.5] 107.0 (34.5), [82.2Y131.7] 36.6 (11.2), [28.5Y44.6]
Posttest
a
Pretest
Posttest
TOT_ST, n = 10
1.0 (0/3.0), [0.2Y1.7]
1.0 (0/3.0), [0.2Y1.7]
3.41 (1.31), 4.50 (1.54), [2.4Y4.3] [3.4Y5.5] 16.4 (5.5), 21.56 (6.1), [12.4Y20.3] [17.0Y25.9] 105.5 (33.6), 128.03 (38.2), [81.4Y129.5] [100.6Y155.3] 34.5 (.9.0), 41.7 (10.4), [28.0Y41.0] [34.2Y49.1]
Scores
Z = 0.00, P = 1.0
t = j10.47, P = 0.001 t = j13.47, P = 0.001 t = j7.48, P = 0.001 t = j8.18, P = 0.001
P
a
21
6
0
22
10
0
33
30
Post-Pre, %
TOT_ST, n = 10
19
9
Post-Pre, %
TOT, n = 10
Change Scores, (%)
U = 5.50, P = 1.000
U = 0.0001, P = 0.001 U = 25.0, P = 0.057 U = 18.0, P = 0.015 U = 5.5, P = 0.001
Pb
Values are presented as median (min/max) or mean (SD), [95% confidence interval]. Paired samples tests and Wilcoxon’s test were used for intragroup comparisons. For intergroup comparisons, Mann-Whitney U test was performed. a Within-group comparison. b Between-group comparison.
Strength Measures in the Paretic Side Shoulder flexors, kg 3.4 (1.2), [2.5Y4.3] Hand grip, lbs 15.5 (7.3), [10.2Y20.7] Active 95.9 (33.1), shoulder ROM [72.1Y119.6] 35.0 (11.8), Fugl-Meyer [26.5Y43.5] Scale motor function (66) Muscle tone (Modified 1.0 (0/3.0), Ashworth Scale, 0Y4) [0.2Y1.6]
Pretest
TOT, n = 10
TABLE 3 Clinical secondary measurements
and parametric data analyses between groups, respectively. The Wilcoxon’s signed-rank test and paired t tests were performed to determine differences within groups. SPSS 16.0 (Statistical Package for the Social Sciences, Inc, Chicago) was used for data analysis. Significance was set at P G 0.05.
RESULTS Study Sample A total of 218 patients were screened, of whom 20 met the study criteria. These patients were randomly allocated in the two experimental groups as follows: ten to the TOT group (n = 10) and ten to the TOT_ST group (n = 10). All patients completed the proposed protocol and were conducted to the revaluation (as depicted in Fig. 1).
Participants’ Characteristics The subjects’ characteristics are shown in Table 1. In summary, the mean (SD) age of the total study sample was 70.4 (7.83) yrs (13 women and 7 men). Mean (SD) time after stroke was 41.4 (11.89) mos. In 75% of the sample, stroke occurred in the left hemisphere, affecting the right side of the body. There were no significant differences between groups for any of the baseline characteristics (Tables 2, 3). This sample was classified as mild-to-moderate impairment according to the Fugl-Meyer Scale (scores between 30 and 50).18,24
Primary Outcome Measure The Upper Extremity Performance Test (TEMPA) The primary outcome measure (TEMPA) demonstrated better values in the bilateral functional graduate (median [min/max] at preevaluation and postevaluation, j2.0 [j9/0] to j1.0 [j6/0] for the TOT group and j4.0 [j6/0] to 0 [j3/0] for the TOT_ST group; P = 0.049) and in the unilateral total score tasks analysis at the end of the treatment (median [min/max] at preevaluation and postevaluation, j19.5 [j60/0] to j15.0 [j60/0] for the TOT group and j21.5 [j60/j12] to j12.5 [j55/0] for the TOT_ST group; P = 0.041) for the TOT_ST group compared with the TOT group. When analyzing within-group scores obtained by TEMPA, both the TOT and TOT_ST groups showed improvements in all posttest scores (Table 2) throughout the intervention period.
Secondary Outcome Measures The secondary outcome measures demonstrated that the TOT_ST group improved when compared www.ajpmr.com
with the TOT group in most of the parameters evaluated. The posttest scores were greater for glenohumeral forward flexion strength (P = 0.001) in the TOT_ST group when compared with the TOT group. Similarly, active shoulder ROM (P = 0.015) and the parameters evaluated with the Fugl-Meyer Scale (P = 0.001) were superior in the TOT_ST group. No differences were observed between groups in handgrip muscle force and muscle tone at the end of the treatment, as evaluated by means of the Modified Ashworth Scale (P 9 0.05). In addition, differences were not noted across time (before vs. after intragroup evaluation) (Table 3).
DISCUSSION The findings of this study support the hypothesis that task-oriented activity combined with strength training is more effective than task-oriented activity alone for inducing neuromuscular adaptations that enhance power production, motor skills, and functional recovery in the chronic phase after stroke. Although both groups showed significant improvement after treatment, the main analysis between groups demonstrated superior performance in the TOT_ST group regarding the functional graduation of bilateral tasks and unilateral total score of the TEMPA, glenohumeral forward flexion strength, active shoulder ROM, and components of motor impairment assessed by means of the Fugl-Meyer Scale. In recent years, task-oriented therapy has been widely used for the rehabilitation of patients in the acute or chronic stage after stroke.19 Several studies have demonstrated the greater benefits of TOT on motor and functional recovery of the upper and lower limbs compared with rehabilitation through conventional exercises, performed without functional goals.18,25Y27 The task-oriented therapy approach meets the individual’s preferences and has been shown to increase motor skills in the upper limbs after stroke. The effectiveness of TOT is evident in lower-limb rehabilitation, when gait is practiced using a functional approach. Intensive muscle training associated with functional activities can induce improvement in gait, gait-related tasks, and walking competency.28,29 In the present study, improvements in functional activities were observed in both groups (TOT and TOT_ST) after training, as assessed by means of the primary outcome measure scale (TEMPA). It is well known that learning a new motor skill involves plastic modifications related to motor learning and that these changes are proportional to the complexity of the learned task and level of motor activity Strength Training in Elderly Patients Post-Stroke
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required.30 This might explain the significantly greater variation in scores of unilateral tasks as well as in the aspects related to the quality of bilateral movements in the TOT_ST group. As in the chronic stage after stroke, peripheral muscle changes occur, and weakness is prevalent; studies have shown that sufficient strength in the upper limbs is related to the ability to adequately perform many motor activities.2 At the end of the rehabilitation program, significant strength gains were observed for both groups (TOT and TOT_ST). Strength training performed by the TOT_ST group enhanced glenohumeral forward flexion strength, as expected. Muscle strengthening using dynamic (isotonic) exercises leads to a significant improvement in grip strength and function for patients in the subacute and chronic phases of stroke. It also seems to be more favorable for people with moderate sensorimotor damage, and no adverse effects such as pain or increase of muscle tone have been noted.31 Although studies addressing the upper limbs are limited, it has been demonstrated that the inclusion of strengthening exercises for lower limb rehabilitation after stroke results in increased strength, speed, and quality of movement. It has also been shown to increase static and dynamic balance and motor performance.32 However, strengthening exercises have not been shown to change muscle tone in the trained segment.33 Glenohumeral forward flexion and handgrip are the best predictors of the upper-limb function after stroke and therefore were chosen for assessment and training.34 Thus, considering the increased strength gain, it was expected that the enhancement in active ROM would also be higher in the TOT_ST group. Active ROM is extremely important for motor function in the upper limbs and is usually impaired in patients with hemiparesis because of muscle weakness as well as abnormal and synergistic patterns of muscle recruitment.35 Motor function evaluation, assessed by means of the Fugl-Meyer Scale, demonstrated higher variation in scores on reevaluation in the TOT_ST group compared with the TOT group. This scale is the main tool used for measuring motor impairment after stroke and assesses the presence of isolated vs. synergistic patterns of movement.35 This leads the authors to assume that TOT, when performed together with strength training, is more effective for the rehabilitation of upper-limb motor function compared with TOT alone. A limitation of the study results is the relatively small sample size. This prevents the ability to generalize the results to all chronic stroke patients. Second, no long-term evaluation was made. Future
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studies need to verify the long-term effect of taskoriented activities associated with strength training on motor skill and activity improvements. Specifically, research should examine changes in extension force of the hand and elbow and verify the effects of rehabilitation parameters such as dose and intensity of the intervention. Finally, examining the effects in patients with multiple strokes would be beneficial. Task-oriented therapy is based on the practice of functional activities performed in a real context that aims to acquire strategies for motion control. The TOT works with clear functional goals, which can increase efficiency and effectiveness in rehabilitation after stroke. It also functions to optimize learning and encourage transfer to activities of daily living.36 This study presented positive results of TOT for the rehabilitation of upper limbs in chronic stroke patients. Thus, muscle strength training is a pivotal component of upper-limb rehabilitation, as demonstrated by the superior scores achieved by the TOT_ST group in most of the evaluated parameters. The authors believe that these findings have important implications to the clinical approach for stroke rehabilitation, therefore contributing to evidence-based practice. Clearly, more experimental studies are needed to clarify the longterm effects of task-oriented strength training for chronic patients with mild impairment after stroke. ACKNOWLEDGMENTS
ScienceDocs, Inc, provided English editing of the manuscript. REFERENCES 1. Shelton FN, Reding MJ: Effect of lesion location on upper limb motor recovery after stroke. Stroke 2001; 32:107Y12 2. Harris JE, Eng JJ: Strength training improves upperlimb function in individuals with stroke: A metaanalysis. Stroke 2010;41:136Y40 3. Prado-Medeiros CL, Silva MP, Lessi GC, et al: Muscle atrophy and functional deficits of knee extensors and flexors in people with chronic stroke. Phys Ther 2012; 92:429Y39 4. Patten C, Lexell J, Brown HE: Weakness and strength training in persons with poststroke hemiplegia: Rationale, method, and efficacy. J Rehabil Res Dev 2004; 41:293Y312 5. Kamper DG, Fischer HC, Cruz EG, et al: Weakness is the primary contributor to finger impairment in chronic stroke. Arch Phys Med Rehabil 2006;87: 1262Y9 6. Canning CG, Ada L, Adams R, et al: Loss of strength contributes more to physical disability after stroke than loss of dexterity. Clin Rehabil 2004;18:300Y8
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7. Andrews AW, Bohannon RW: Decreased shoulder range of motion on paretic side after stroke. Phys Ther 1989;69:768Y72 8. Triandafilou KM, Fischer HC, Towles JD, et al: Diminished capacity to modulate motor activation patterns according to task contributes to thumb deficits following stroke. J Neurophysiol 2011;106: 1644Y51 9. Cruz EG, Waldinger HC, Kamper DG: Kinetic and kinematic workspaces of the index finger following stroke. Brain 2005;128(pt 5):1112Y21 10. Ryan AS, Buscemi A, Forrester L, et al: Atrophy and intramuscular fat in specific muscles of the thigh: Associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 2011;25:865Y72 11. Lieber RL, Steinman S, Barash IA, et al: Structural and functional changes in spastic skeletal muscle. Muscle Nerve 2004;29:615Y27 12. Ryan AS, Dobrovolny CL, Smith GV, et al: Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 2002;83: 1703Y7 13. Andersen LL, Zeeman P, Jorgensen JR, et al: Effects of intensive physical rehabilitation on neuromuscular adaptations in adults with poststroke hemiparesis. J Strength Cond Res 2011;25:2808Y17 14. Flansbjer UB, Lexell J, Brogardh C: Long-term benefits of progressive resistance training in chronic stroke: A 4-year follow-up. J Rehabil Med 2012;44:218Y21 15. Hammami N, Coroian FO, Julia M, et al: Isokinetic muscle strengthening after acquired cerebral damage: A literature review. Ann Phys Rehabil Med 2012; 55:279Y91 16. Timmermans AA, Seelen HA, Geers RP, et al: Sensorbased arm skill training in chronic stroke patients: Results on treatment outcome, patient motivation, and system usability. IEEE Trans Neural Syst Rehabil Eng 2010;18:284Y92 17. Van Peppen RP, Kwakkel G, Wood-Dauphinee S, et al: The impact of physical therapy on functional outcomes after stroke: What’s the evidence? Clin Rehabil 2004;18:833Y62 18. Michaelsen SM, Dannenbaum R, Levin MF: Taskspecific training with trunk restraint on arm recovery in stroke: Randomized control trial. Stroke 2006; 37:186Y92 19. Timmermans AA, Spooren AI, Kingma H, et al: Influence of task-oriented training content on skilled arm-hand performance in stroke: A systematic review. Neurorehabil Neural Repair 2010;24:858Y70 20. Michaelsen SM, Luta A, Roby-Brami A, et al: Effect of trunk restraint on the recovery of reaching movements in hemiparetic patients. Stroke 2001;32:1875Y83 21. Michaelsen SM, Natalio MA, Silva AG, et al: Reliability of the translation and adaptation of the Test d’E´valuation des Membres Supe´rieurs des Personnes Aˆge´es (TEMPA) to the Portuguese language and validation
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for adults with hemiparesis. Rev Bras Fisioter 2008;12:9 22. Bohannon RW, Smith MB: Assessment of strength deficits in eight paretic upper extremity muscle groups of stroke patients with hemiplegia. Phys Ther 1987; 67:522Y5 23. Desrosiers J, Hebert R, Bravo G, et al: Upper extremity performance test for the elderly (TEMPA): Normative data and correlates with sensorimotor parameters. Test d’Evaluation des Membres Superieurs de Personnes Agees. Arch Phys Med Rehabil 1995; 76:1125Y9 24. Cheung VC, Turolla A, Agostini M, et al: Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci U S A 2012; 109:14652Y6 25. Higgins J, Salbach NM, Wood-Dauphinee S, et al: The effect of a task-oriented intervention on arm function in people with stroke: A randomized controlled trial. Clin Rehabil 2006;20:296Y310 26. Morris JH, van Wijck F, Joice S, et al: A comparison of bilateral and unilateral upper-limb task training in early poststroke rehabilitation: A randomized controlled trial. Arch Phys Med Rehabil 2008;89:1237Y45 27. Rensink M, Schuurmans M, Lindeman E, et al: Taskoriented training in rehabilitation after stroke: Systematic review. J Adv Nurs 2009;65:737Y54 28. Salbach NM, Mayo NE, Wood-Dauphinee S, et al: A task-orientated intervention enhances walking distance and speed in the first year post stroke: A randomized controlled trial. Clin Rehabil 2004;18:509Y19 29. Outermans JC, van Peppen RP, Wittink H, et al: Effects of a high-intensity task-oriented training on gait performance early after stroke: A pilot study. Clin Rehabil 2010;24:979Y87 30. Hosp JA, Luft AR: Cortical plasticity during motor learning and recovery after ischemic stroke. Neural Plast 2011;2011:871296 31. Harris JE, Eng JJ: Paretic upper-limb strength best explains arm activity in people with stroke. Phys Ther 2007;87:88Y97 32. Weiss A, Suzuki T, Bean J, et al: High intensity strength training improves strength and functional performance after stroke. Am J Phys Med Rehabil 2000; 79:369Y76 33. Sharp SA, Brouwer BJ: Isokinetic strength training of the hemiparetic knee: Effects on function and spasticity. Arch Phys Med Rehabil 1997;78:1231Y6 34. Mercier C, Bourbonnais D: Relative shoulder flexor and handgrip strength is related to upper limb function after stroke. Clin Rehabil 2004;18:215Y21 35. Roh J, Rymer WZ, Perreault EJ, et al: Alterations in upper limb muscle synergy structure in chronic stroke survivors. J Neurophysiol 2013;109:768Y81 36. Wade DT: Goal setting in rehabilitation: An overview of what, why and how. Clin Rehabil 2009;23:291Y5
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19
Affiliations:
Stroke
ORIGINAL RESEARCH ARTICLE
From the Programa de Po´s-graduac¸a˜o em Cieˆncias da Reabilitac¸a˜o (PBdS, FNA, FC, ASP), Departamento de Fisioterapia (PG, FC, ASP), and Programa de Po´s Graduac¸a˜o em Cieˆncias da Sau´de (ASP), Universidade Federal de Cieˆncias da Sau´de de Porto Alegre, Porto Alegre, Rio Grande do Sul, Brazil.
Correspondence: All correspondence and requests for reprints should be addressed to: Aline de Souza Pagnussat, PhD, Departamento de Fisioterapia, Universidade Federal de Cieˆncias da Sau´de de Porto Alegre, Rua Sarmento Leite, 245, 90050-170, Porto Alegre, RS, Brazil.
Disclosures: Supported by grants from the Brazilian agencies CNPq (National Council of Technological and Scientific, Brazil) and the National Council for the Improvement of Higher Education (CAPES-Brazil). 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.
0894-9115/15/9401-0011 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000135
Strength Training Associated with Task-Oriented Training to Enhance Upper-Limb Motor Function in Elderly Patients with Mild Impairment After Stroke A Randomized Controlled Trial ABSTRACT da Silva PB, Antunes FN, Graef P, Cechetti F, Pagnussat AS: Strength training associated with task-oriented training to enhance upper-limb motor function in elderly patients with mild impairment after stroke: a randomized controlled trial. Am J Phys Med Rehabil 2015;94:11Y19.
Objective: The aim of this study was to verify the effects of loaded exercises associated with a task-oriented training (TOT) program in the recovery of upperlimb function in individuals with chronic hemiparesis after stroke. Design: This study used a single-blinded, randomized controlled trial. Patients were included into two TOT groups: one that performed the task-oriented therapy without load (TOT group, n = 10) and another one that performed task-oriented therapy with personalized resistance (TOT_ST group, n = 10) for 6 wks, for a total of 12 sessions. Main measures included The Upper Extremity Performance Test, shoulder flexor and handgrip strength, shoulder active range of motion, motor impairment (Fugl-Meyer Scale), and muscle tone.
Results: The TOT_ST group demonstrated better scores relating to unilateral tasks and in the quality aspects of bilateral movements (The Upper Extremity Performance Test, P = 0.04) at the end of rehabilitation protocol. The highest muscle force gain was reached by the TOT_ST group for the shoulder flexors (P = 0.001). Similarly, the active range of motion (P = 0.01) and Fugl-Meyer scores (P = 0.001) were higher in the TOT_ST group compared with the TOT group. Both groups showed improvement after training.
Conclusions: Strength training was able to intensify the upper-limb rehabilitation, as demonstrated by the superior scores achieved by the TOT_ST group in most of the evaluated parameters. Muscle strength training might be a pivotal element of the task-oriented rehabilitation program of chronic patients with mild impairment after stroke. Key Words:
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Chronic Hemiparesis, Physiotherapy, Rehabilitation, Muscle Weakness
Strength Training in Elderly Patients Post-Stroke Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
11
C
hronic diseases are the major cause of death and disability worldwide. Among these disorders, stroke is the leading cause of long-term physical impairment. The most prominent motor deficit after stroke is paresis of the side of the body contralateral to the cerebrovascular event, which can permanently affect arm-hand performance.1 Contemporary research has demonstrated weakness as one of the most important primary impairments in persons after stroke. Weakness has been shown to compromise many meaningful daily tasks and greatly affects participation and qualityof-life of individuals with hemiparesis.2Y5 Weakness has been reported as decreased torque generation at the elbow,6 shoulder,7 fingers, and thumb,5,8,9 which can be a consequence of an abnormal motor activation and/or physical inactivity. A disabling stroke combined with a sedentary lifestyle accelerates the gradual loss of muscle mass and magnifies the usual age-associated loss of fat-free mass, which consequently leads to functional deficits.10 The decrease in muscle strength can occur as a consequence of structural and functional changes in spastic muscles. These modifications include altered muscle fiber size, fiber type distribution, proliferation of extracellular matrix material, increased stiffness of spastic muscle cells, and inferior mechanical properties of extracellular content.11,12 In the chronic phase after a stroke, strengthening interventions can maximize the capacity for voluntary neuromuscular activation. This increased muscle strength might be able to promote functional improvement and potentially improve quality-of-life without negative adverse effects (such as the increase of hypertonia and pain).4,13,14 Accordingly, methods consisting of strength and endurance training are now part of the programs regularly offered to patients after stroke.15 There are several research studies that document the effectiveness of task-oriented training (TOT) as a neurologic treatment approach.16Y18 An ideal task-oriented protocol should be composed of unilateral and bilateral activities geared toward a clear functional goal (similar to activities of daily living using real-life objects) and performed in a contextspecific environment.19 Although the resistance training could be an effective training method to improve and maintain muscle strength in the short term and long term during stroke rehabilitation,14 a patient-customized training load is not always a part of the task-oriented rehabilitation program. Several studies using TOT protocols have been conducted without specifically including strength training.19
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da Silva et al.
Considering that post-stroke patients are likely to benefit from rehabilitation interventions that maximize the capacity for voluntary neuromuscular activation, the aim of this study was to determine the effectiveness of a patient-customized training load as part of the task-oriented upper-limb rehabilitation program in individuals with chronic hemiparesis and mild impairment after stroke. It was hypothesized that muscle strength training could be a pivotal element of the task-oriented rehabilitation program. Strength training might be more effective in improving muscle strength, motor skills, and functional recovery during short-term stroke rehabilitation.
METHODS Participants This prospective, randomized controlled trial was registered and allocated by the Brazilian Clinical Trials Registry and included concealed randomization and blinded assessments. In all, 218 adults with chronic hemiparesis were screened, and 20 of them were recruited from two medical centers during 18 mos (Fig. 1). Participants provided informed written consent to a protocol approved by the Universidade Federal de Cieˆncias da Sau´de de Porto Alegre’s Human Research Ethics Committee (protocol number 11-826). The inclusion criteria were (1) time since the onset of a single, unilateral stroke ranging between 6 mos and 5 yrs (chronic stage); (2) ability to comprehend simple instructions (Mini-Mental State Examination with a minimum score of 20); (3) no pain, contractures, or severe weakness in the shoulder muscles (G3 in the Manual Muscular Testing or lack of ability to perform 60 degrees of active shoulder range of motion [ROM] against the gravity); and (4) not submitted to other upper-limb rehabilitation programs during the participation in this study. Participants were excluded if they had (1) other neurologic, neuromuscular, or orthopedic disease; (2) severe comorbidities; or (3) severe spasticity of the elbow flexors that compromised the task performance (93 points according to the Modified Ashworth Scale).
Study Design During the 6-wk intervention period, patients were included in a rehabilitation protocol composed by task-oriented activity with or without strength training. Patients were stratified based on the strength of glenohumeral forward flexion, which was quantified with a load cell (Miotec, Brazil). The allocation schedule was generated and concealed in sequentially numbered, sealed, opaque envelopes. Random assignment was computer-generated by a physiotherapist
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FIGURE 1 Subject recruitment and attrition flowchart. who was not involved in the patient selection. Participants were randomly assigned to two intervention groupsVtask-oriented without strength training (TOT, n = 10) or task-oriented with strength training (TOT_ST, n = 10)V1 wk before the start of the intervention. Baseline evaluation and postintervention measures were performed by a well-trained research assistant blind to group allocation. Participants received a 30-min, therapist-supervised, home rehabilitation program two times per week for 6 wks (total of 12 sessions). Each session began with a period of slow-sustained stretching and passive ROM of the hemiparetic upper limb, focusing on the tone normalization of the elbow and wrist flexors and shoulder abductors. Rehabilitation exercises were performed with subjects seated in a chair, which allowed for a posture in which the knees and hips were maintained at 90 degrees. A belt was used to restrain the trunk and avoid compensatory movements.20 The load determination for the strength protocol was based on the ability to generate maximal force during www.ajpmr.com
glenohumeral forward flexion on the hemiparetic side. The load used for training remained at 60% of the maximum value during the entire rehabilitation period.
Intervention The rehabilitation protocol consisted of five taskoriented movements chosen to meet the following criteria: unilateral (only the paretic limb) and bilateral functional exercises (both upper limbs used to perform the task), activity-of-daily-living goal, contextspecific environment using real-life object manipulation, and exercised in multiple movement planes. Rehabilitation exercises simulated the following activities of daily living: brushing hair, putting on a scarf, feeding, handling a coffee pot, and putting a pot on a high cabinet shelf. All activities were performed with increasing difficulty levels (progression in ROM according to the patient capacity), followed with feedback of the exercise performance, and reinforced by verbal instructions. Strength Training in Elderly Patients Post-Stroke
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Both groups received the same number and frequency of sessions, which consisted of ten repetitions of the same movement with a 3-min resting period between each movement. The TOT and TOT_ST groups randomly performed all of the five tasks each day. Patients from the TOT_ST group performed all tasks with load resistance (60% of the maximum baseline force) put on the arm as a bracelet or into a jug. Both groups’ rehabilitation was performed at home. The execution of the exercises was always supervised by a physiotherapist. Two physiotherapists conducted the rehabilitation protocol for patients from both groups. Therapists received training by the same instructor and used similar verbal cues for patients in both groups.
Outcome Measures The primary clinical outcome measure for improving upper-limb performance in unilateral and bilateral activities was the Test d’Evaluatio´n des Membres Superieus des Personnes Age´es (TEMPA).21 This test was used to evaluate the performance of the upper limb in the completion of functional activities. The Brazilian version of the TEMPA is a protocol for the observation of upper-limb performance composed of eight standardized tasks (four bilateral and four unilateral ones), which represent daily activities. Each task was evaluated by three criteria: speed of execution, functional levels or functional graduation, and analyses of the performed tasks. The functional level or functional graduation refers to the individual’s autonomy in each task measured on a four-level scale as follows: tasks (0) were successfully completed without hesitation or difficulty; (j1) were completed, but with some difficulty; (j2) were partially executed or some steps were performed with significant difficulty; and (j3) failed to be completed, even if any degree of assistance was offered. The analyses of the performed tasks quantified the difficulties experienced by the subjects according to five dimensions related to upper-extremity sensory motor
skills: strength, ROM, precision of gross movements, prehension, and precision of fine movements. The total scores were determined by adding the scores obtained from both the unilateral and bilateral tasks. The higher score represents the best performance, ranging from 0 to j150. Adequate reliability has been reported using the TEMPA scale for adults with hemiparesis.21 Secondary outcome measures included shoulder and grip strength (in kilograms and pounds, respectively), active shoulder ROM (degrees), motor recovery of the upper limbs, and muscle tone. Three grip and shoulder strength measures were taken using the Jamar hydraulic hand dynamometer (Sammons Preston Corp) and load cell (Miotec, Brazil), respectively, with standardized positioning and instruction. The highest score of the three trials was retained. Standard goniometry was used to measure active glenohumeral forward flexion ROM. Motor recovery of the upper limbs was evaluated using the upperextremity session of the Fugl-Meyer assessment scale. The Fugl-Meyer Scale includes four motor subitems relevant to the involved upper extremity: (1) shoulder/ elbow/forearm, (2) wrist, (3) hand, and (4) speed coordination. Each item was rated on a 3-point scale (0, cannot perform; 1, partially performed; 2, fully performed) for a 66-point maximum. The Modified Ashworth Scale22 was used to evaluate the elbow flexors’ muscle tone.
Statistical Analysis The sample size was determined to detect group differences of 3 points in the primary clinical outcome scale (TEMPA, unilateral task analysis subsection), with a power of 70% for a two-tailed t test with significance set at a level of 0.05.23 Results are presented as median (minimum/maximum) or mean (SD). Data normality was tested using the ShapiroWilk test, and the homogeneity of variance was tested by Levene statistic. The Mann-Whitney U test and independent samples t test were used for nonparametric
TABLE 1 Characteristics of the participants
Sex, n (%) Male Female Paretic side, n (%) Right Left Age, mean (SD), yrs Time since onset, mean (SD), mos a
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da Silva et al.
TOT, n = 10
TOT_ST, n = 10
4 (40) 6 (60)
3 (30) 7 (70)
3 (30) 7 (70) 70.4 (7.83) 41.4 (11.89)
2 (20) 8 (80) 70.3 (7.83) 40.2 (13.48)
Pa
1.000 1.000 t = 0.03, P = 0.978 t = 0.2, P = 0.835
Fisher’s exact test for proportions. t test for continuous variables.
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Strength Training in Elderly Patients Post-Stroke
Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
15
Pretest
Posttest
j15 (j48/j9), j9.0 (j44.0/0), [j33.0 to j7.0] [j32.4 to j4.5] j14 (j22/0), j4.5 (j17/0), [j16.0 to j2.7] [j13.3 to j1.0] j21.5 (j60/j12), j12.5 (j55/0), [j41.4 to j7.5] [j23.2 to j40.7] j19.0 (j27/0), j4.5 (j19/0), [j19.3 to j2.4] [j16.8 to j0.9] j39.0 (j84/j10), j16.0 (j72/0), [j60.4 to j13.0] [j56.4 to j8.7]
Z = j2.54, P = 0.011 Z = j2.54, P = 0.011 Z = j2.54, P = 0.011 Z = j2.53, P = 0.012 Z = j2.66, P = 0.008
j1.0 (j11/0), [j5.4 to j0.5] 0 (j3/0), [j3.5 to 0.1]
Posttest
j4.5 (j12/j3), [j7.9 to j3.6] j4.0 (j6/0), [j3.4 to 0.4]
Pretest
TOT_ST, n = 10
Z = j2.27, P = 0.023 Z = 2.23, P = 0.025
Pa
Scores
Z = j2.67, P = 0.008 Z = j2.52, P = 0.012 Z = j2.81, P = 0.005 Z = j2.53, P = 0.011 Z = j2.81, P = 0.005
Z = j2.53, P = 0.012 Z = j2.56, P = 0.011
Pa
42 31 42 41 45
25 13 28 17
73
29 8
71
Post-Pre, % 15
Post-Pre, %
TOT, n = 10 TOT_ST, n = 10
Change Scores, %
Values are presented as median (min/max), [95% confidence interval]. Wilcoxon’s and Mann-Whitney U tests were used for intragroup and intergroup comparisons, respectively. a Within-group comparison. b Between-group comparison.
Functional Graduate Unilateral tasks j4.0 (j12/0), j3.0 (j12/0), [j8.2 to j2.1] [j7.1 to j1.2] Bilateral tasks j2.0 (j9/0), j1.0 (j6/0), [j2.0 to 0.06] [j0.9 to 0.1] Task Analysis Unilateral tasks j15.5 (j48/0), j12.0 (j48/0), [j25.7 to j5.0] [j23.3 to j2.2] Bilateral tasks j8.0 (j40/0), j5.5 (j34/0), [j13.1 to j1.8] [j11.5 to 0.1] Unilateral j19.5 (j60/0), j15.0 (j60/0), total score [j32.6 to j6.7] [j29.9 to j3.0] Bilateral j10.0 (j49/0), j6.0 (j40/0), total score [j15.1 to j1.8] [j12.4 to 0.2] j27.0 (j109/j105), j21.5 (j92/j1), Unilateral and [j47.3 to j9.6] [j41.9 to j3.2] bilateral tasks’ scores combined
TEMPA
TOT, n = 10
TABLE 2 Clinical primary measurements
U = 27.0, P = 0.082 U = 44.0, P = 0.648 U = 23.0, P = 0.041 U = 41.0, P = 0.490 U = 32.5, P = 0.186
U = 31.5, P = 0.156 U = 24.5, P = 0.049
Pb
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t = j3.70, P = 0.004 t = 4.86, P = 0.001 t = j5.06, P = 0.001 t = j2.38, P = 0.041 Z = 0.00, P = 1.0
1.0 (0/3.0), [0.2Y1.6]
P
3.6 (1.4), [2.6Y4.6] 17.6 (6.9), [12.6Y22.5] 107.0 (34.5), [82.2Y131.7] 36.6 (11.2), [28.5Y44.6]
Posttest
a
Pretest
Posttest
TOT_ST, n = 10
1.0 (0/3.0), [0.2Y1.7]
1.0 (0/3.0), [0.2Y1.7]
3.41 (1.31), 4.50 (1.54), [2.4Y4.3] [3.4Y5.5] 16.4 (5.5), 21.56 (6.1), [12.4Y20.3] [17.0Y25.9] 105.5 (33.6), 128.03 (38.2), [81.4Y129.5] [100.6Y155.3] 34.5 (.9.0), 41.7 (10.4), [28.0Y41.0] [34.2Y49.1]
Scores
Z = 0.00, P = 1.0
t = j10.47, P = 0.001 t = j13.47, P = 0.001 t = j7.48, P = 0.001 t = j8.18, P = 0.001
P
a
21
6
0
22
10
0
33
30
Post-Pre, %
TOT_ST, n = 10
19
9
Post-Pre, %
TOT, n = 10
Change Scores, (%)
U = 5.50, P = 1.000
U = 0.0001, P = 0.001 U = 25.0, P = 0.057 U = 18.0, P = 0.015 U = 5.5, P = 0.001
Pb
Values are presented as median (min/max) or mean (SD), [95% confidence interval]. Paired samples tests and Wilcoxon’s test were used for intragroup comparisons. For intergroup comparisons, Mann-Whitney U test was performed. a Within-group comparison. b Between-group comparison.
Strength Measures in the Paretic Side Shoulder flexors, kg 3.4 (1.2), [2.5Y4.3] Hand grip, lbs 15.5 (7.3), [10.2Y20.7] Active 95.9 (33.1), shoulder ROM [72.1Y119.6] 35.0 (11.8), Fugl-Meyer [26.5Y43.5] Scale motor function (66) Muscle tone (Modified 1.0 (0/3.0), Ashworth Scale, 0Y4) [0.2Y1.6]
Pretest
TOT, n = 10
TABLE 3 Clinical secondary measurements
and parametric data analyses between groups, respectively. The Wilcoxon’s signed-rank test and paired t tests were performed to determine differences within groups. SPSS 16.0 (Statistical Package for the Social Sciences, Inc, Chicago) was used for data analysis. Significance was set at P G 0.05.
RESULTS Study Sample A total of 218 patients were screened, of whom 20 met the study criteria. These patients were randomly allocated in the two experimental groups as follows: ten to the TOT group (n = 10) and ten to the TOT_ST group (n = 10). All patients completed the proposed protocol and were conducted to the revaluation (as depicted in Fig. 1).
Participants’ Characteristics The subjects’ characteristics are shown in Table 1. In summary, the mean (SD) age of the total study sample was 70.4 (7.83) yrs (13 women and 7 men). Mean (SD) time after stroke was 41.4 (11.89) mos. In 75% of the sample, stroke occurred in the left hemisphere, affecting the right side of the body. There were no significant differences between groups for any of the baseline characteristics (Tables 2, 3). This sample was classified as mild-to-moderate impairment according to the Fugl-Meyer Scale (scores between 30 and 50).18,24
Primary Outcome Measure The Upper Extremity Performance Test (TEMPA) The primary outcome measure (TEMPA) demonstrated better values in the bilateral functional graduate (median [min/max] at preevaluation and postevaluation, j2.0 [j9/0] to j1.0 [j6/0] for the TOT group and j4.0 [j6/0] to 0 [j3/0] for the TOT_ST group; P = 0.049) and in the unilateral total score tasks analysis at the end of the treatment (median [min/max] at preevaluation and postevaluation, j19.5 [j60/0] to j15.0 [j60/0] for the TOT group and j21.5 [j60/j12] to j12.5 [j55/0] for the TOT_ST group; P = 0.041) for the TOT_ST group compared with the TOT group. When analyzing within-group scores obtained by TEMPA, both the TOT and TOT_ST groups showed improvements in all posttest scores (Table 2) throughout the intervention period.
Secondary Outcome Measures The secondary outcome measures demonstrated that the TOT_ST group improved when compared www.ajpmr.com
with the TOT group in most of the parameters evaluated. The posttest scores were greater for glenohumeral forward flexion strength (P = 0.001) in the TOT_ST group when compared with the TOT group. Similarly, active shoulder ROM (P = 0.015) and the parameters evaluated with the Fugl-Meyer Scale (P = 0.001) were superior in the TOT_ST group. No differences were observed between groups in handgrip muscle force and muscle tone at the end of the treatment, as evaluated by means of the Modified Ashworth Scale (P 9 0.05). In addition, differences were not noted across time (before vs. after intragroup evaluation) (Table 3).
DISCUSSION The findings of this study support the hypothesis that task-oriented activity combined with strength training is more effective than task-oriented activity alone for inducing neuromuscular adaptations that enhance power production, motor skills, and functional recovery in the chronic phase after stroke. Although both groups showed significant improvement after treatment, the main analysis between groups demonstrated superior performance in the TOT_ST group regarding the functional graduation of bilateral tasks and unilateral total score of the TEMPA, glenohumeral forward flexion strength, active shoulder ROM, and components of motor impairment assessed by means of the Fugl-Meyer Scale. In recent years, task-oriented therapy has been widely used for the rehabilitation of patients in the acute or chronic stage after stroke.19 Several studies have demonstrated the greater benefits of TOT on motor and functional recovery of the upper and lower limbs compared with rehabilitation through conventional exercises, performed without functional goals.18,25Y27 The task-oriented therapy approach meets the individual’s preferences and has been shown to increase motor skills in the upper limbs after stroke. The effectiveness of TOT is evident in lower-limb rehabilitation, when gait is practiced using a functional approach. Intensive muscle training associated with functional activities can induce improvement in gait, gait-related tasks, and walking competency.28,29 In the present study, improvements in functional activities were observed in both groups (TOT and TOT_ST) after training, as assessed by means of the primary outcome measure scale (TEMPA). It is well known that learning a new motor skill involves plastic modifications related to motor learning and that these changes are proportional to the complexity of the learned task and level of motor activity Strength Training in Elderly Patients Post-Stroke
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required.30 This might explain the significantly greater variation in scores of unilateral tasks as well as in the aspects related to the quality of bilateral movements in the TOT_ST group. As in the chronic stage after stroke, peripheral muscle changes occur, and weakness is prevalent; studies have shown that sufficient strength in the upper limbs is related to the ability to adequately perform many motor activities.2 At the end of the rehabilitation program, significant strength gains were observed for both groups (TOT and TOT_ST). Strength training performed by the TOT_ST group enhanced glenohumeral forward flexion strength, as expected. Muscle strengthening using dynamic (isotonic) exercises leads to a significant improvement in grip strength and function for patients in the subacute and chronic phases of stroke. It also seems to be more favorable for people with moderate sensorimotor damage, and no adverse effects such as pain or increase of muscle tone have been noted.31 Although studies addressing the upper limbs are limited, it has been demonstrated that the inclusion of strengthening exercises for lower limb rehabilitation after stroke results in increased strength, speed, and quality of movement. It has also been shown to increase static and dynamic balance and motor performance.32 However, strengthening exercises have not been shown to change muscle tone in the trained segment.33 Glenohumeral forward flexion and handgrip are the best predictors of the upper-limb function after stroke and therefore were chosen for assessment and training.34 Thus, considering the increased strength gain, it was expected that the enhancement in active ROM would also be higher in the TOT_ST group. Active ROM is extremely important for motor function in the upper limbs and is usually impaired in patients with hemiparesis because of muscle weakness as well as abnormal and synergistic patterns of muscle recruitment.35 Motor function evaluation, assessed by means of the Fugl-Meyer Scale, demonstrated higher variation in scores on reevaluation in the TOT_ST group compared with the TOT group. This scale is the main tool used for measuring motor impairment after stroke and assesses the presence of isolated vs. synergistic patterns of movement.35 This leads the authors to assume that TOT, when performed together with strength training, is more effective for the rehabilitation of upper-limb motor function compared with TOT alone. A limitation of the study results is the relatively small sample size. This prevents the ability to generalize the results to all chronic stroke patients. Second, no long-term evaluation was made. Future
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studies need to verify the long-term effect of taskoriented activities associated with strength training on motor skill and activity improvements. Specifically, research should examine changes in extension force of the hand and elbow and verify the effects of rehabilitation parameters such as dose and intensity of the intervention. Finally, examining the effects in patients with multiple strokes would be beneficial. Task-oriented therapy is based on the practice of functional activities performed in a real context that aims to acquire strategies for motion control. The TOT works with clear functional goals, which can increase efficiency and effectiveness in rehabilitation after stroke. It also functions to optimize learning and encourage transfer to activities of daily living.36 This study presented positive results of TOT for the rehabilitation of upper limbs in chronic stroke patients. Thus, muscle strength training is a pivotal component of upper-limb rehabilitation, as demonstrated by the superior scores achieved by the TOT_ST group in most of the evaluated parameters. The authors believe that these findings have important implications to the clinical approach for stroke rehabilitation, therefore contributing to evidence-based practice. Clearly, more experimental studies are needed to clarify the longterm effects of task-oriented strength training for chronic patients with mild impairment after stroke. ACKNOWLEDGMENTS
ScienceDocs, Inc, provided English editing of the manuscript. REFERENCES 1. Shelton FN, Reding MJ: Effect of lesion location on upper limb motor recovery after stroke. Stroke 2001; 32:107Y12 2. Harris JE, Eng JJ: Strength training improves upperlimb function in individuals with stroke: A metaanalysis. Stroke 2010;41:136Y40 3. Prado-Medeiros CL, Silva MP, Lessi GC, et al: Muscle atrophy and functional deficits of knee extensors and flexors in people with chronic stroke. Phys Ther 2012; 92:429Y39 4. Patten C, Lexell J, Brown HE: Weakness and strength training in persons with poststroke hemiplegia: Rationale, method, and efficacy. J Rehabil Res Dev 2004; 41:293Y312 5. Kamper DG, Fischer HC, Cruz EG, et al: Weakness is the primary contributor to finger impairment in chronic stroke. Arch Phys Med Rehabil 2006;87: 1262Y9 6. Canning CG, Ada L, Adams R, et al: Loss of strength contributes more to physical disability after stroke than loss of dexterity. Clin Rehabil 2004;18:300Y8
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7. Andrews AW, Bohannon RW: Decreased shoulder range of motion on paretic side after stroke. Phys Ther 1989;69:768Y72 8. Triandafilou KM, Fischer HC, Towles JD, et al: Diminished capacity to modulate motor activation patterns according to task contributes to thumb deficits following stroke. J Neurophysiol 2011;106: 1644Y51 9. Cruz EG, Waldinger HC, Kamper DG: Kinetic and kinematic workspaces of the index finger following stroke. Brain 2005;128(pt 5):1112Y21 10. Ryan AS, Buscemi A, Forrester L, et al: Atrophy and intramuscular fat in specific muscles of the thigh: Associated weakness and hyperinsulinemia in stroke survivors. Neurorehabil Neural Repair 2011;25:865Y72 11. Lieber RL, Steinman S, Barash IA, et al: Structural and functional changes in spastic skeletal muscle. Muscle Nerve 2004;29:615Y27 12. Ryan AS, Dobrovolny CL, Smith GV, et al: Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil 2002;83: 1703Y7 13. Andersen LL, Zeeman P, Jorgensen JR, et al: Effects of intensive physical rehabilitation on neuromuscular adaptations in adults with poststroke hemiparesis. J Strength Cond Res 2011;25:2808Y17 14. Flansbjer UB, Lexell J, Brogardh C: Long-term benefits of progressive resistance training in chronic stroke: A 4-year follow-up. J Rehabil Med 2012;44:218Y21 15. Hammami N, Coroian FO, Julia M, et al: Isokinetic muscle strengthening after acquired cerebral damage: A literature review. Ann Phys Rehabil Med 2012; 55:279Y91 16. Timmermans AA, Seelen HA, Geers RP, et al: Sensorbased arm skill training in chronic stroke patients: Results on treatment outcome, patient motivation, and system usability. IEEE Trans Neural Syst Rehabil Eng 2010;18:284Y92 17. Van Peppen RP, Kwakkel G, Wood-Dauphinee S, et al: The impact of physical therapy on functional outcomes after stroke: What’s the evidence? Clin Rehabil 2004;18:833Y62 18. Michaelsen SM, Dannenbaum R, Levin MF: Taskspecific training with trunk restraint on arm recovery in stroke: Randomized control trial. Stroke 2006; 37:186Y92 19. Timmermans AA, Spooren AI, Kingma H, et al: Influence of task-oriented training content on skilled arm-hand performance in stroke: A systematic review. Neurorehabil Neural Repair 2010;24:858Y70 20. Michaelsen SM, Luta A, Roby-Brami A, et al: Effect of trunk restraint on the recovery of reaching movements in hemiparetic patients. Stroke 2001;32:1875Y83 21. Michaelsen SM, Natalio MA, Silva AG, et al: Reliability of the translation and adaptation of the Test d’E´valuation des Membres Supe´rieurs des Personnes Aˆge´es (TEMPA) to the Portuguese language and validation
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for adults with hemiparesis. Rev Bras Fisioter 2008;12:9 22. Bohannon RW, Smith MB: Assessment of strength deficits in eight paretic upper extremity muscle groups of stroke patients with hemiplegia. Phys Ther 1987; 67:522Y5 23. Desrosiers J, Hebert R, Bravo G, et al: Upper extremity performance test for the elderly (TEMPA): Normative data and correlates with sensorimotor parameters. Test d’Evaluation des Membres Superieurs de Personnes Agees. Arch Phys Med Rehabil 1995; 76:1125Y9 24. Cheung VC, Turolla A, Agostini M, et al: Muscle synergy patterns as physiological markers of motor cortical damage. Proc Natl Acad Sci U S A 2012; 109:14652Y6 25. Higgins J, Salbach NM, Wood-Dauphinee S, et al: The effect of a task-oriented intervention on arm function in people with stroke: A randomized controlled trial. Clin Rehabil 2006;20:296Y310 26. Morris JH, van Wijck F, Joice S, et al: A comparison of bilateral and unilateral upper-limb task training in early poststroke rehabilitation: A randomized controlled trial. Arch Phys Med Rehabil 2008;89:1237Y45 27. Rensink M, Schuurmans M, Lindeman E, et al: Taskoriented training in rehabilitation after stroke: Systematic review. J Adv Nurs 2009;65:737Y54 28. Salbach NM, Mayo NE, Wood-Dauphinee S, et al: A task-orientated intervention enhances walking distance and speed in the first year post stroke: A randomized controlled trial. Clin Rehabil 2004;18:509Y19 29. Outermans JC, van Peppen RP, Wittink H, et al: Effects of a high-intensity task-oriented training on gait performance early after stroke: A pilot study. Clin Rehabil 2010;24:979Y87 30. Hosp JA, Luft AR: Cortical plasticity during motor learning and recovery after ischemic stroke. Neural Plast 2011;2011:871296 31. Harris JE, Eng JJ: Paretic upper-limb strength best explains arm activity in people with stroke. Phys Ther 2007;87:88Y97 32. Weiss A, Suzuki T, Bean J, et al: High intensity strength training improves strength and functional performance after stroke. Am J Phys Med Rehabil 2000; 79:369Y76 33. Sharp SA, Brouwer BJ: Isokinetic strength training of the hemiparetic knee: Effects on function and spasticity. Arch Phys Med Rehabil 1997;78:1231Y6 34. Mercier C, Bourbonnais D: Relative shoulder flexor and handgrip strength is related to upper limb function after stroke. Clin Rehabil 2004;18:215Y21 35. Roh J, Rymer WZ, Perreault EJ, et al: Alterations in upper limb muscle synergy structure in chronic stroke survivors. J Neurophysiol 2013;109:768Y81 36. Wade DT: Goal setting in rehabilitation: An overview of what, why and how. Clin Rehabil 2009;23:291Y5
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