Mental Practice and Mirror Therapy Associated with Conventional Physical Therapy Training on the Hemiparetic Upper Limb in Poststroke Rehabilitation: A Preliminary Study Rafael de Almeida Oliveira,1 Paula Cintia dos Santos Vieira,2 Luciane Fernanda Rodrigues Martinho Fernandes, PhD,3 Lislei Jorge Patrizzi, PhD,3 Sabrina Ferreira de Oliveira, MSc,3 and Luciane Aparecida Pascucci Sande de Souza, PhD3 1
Master's program in Physical Education, Federal University of Triângulo Mineiro (UFTM); 2Physiotherapist graduated from UFTM; 3 Department of Physical Therapy, UFTM, Uberaba, Minas Gerais, Brazil Background: The presence of sensory and motor deficits is common in patients post stroke. Mental practice (MP) and mirror therapy (MT) can be used as therapeutic techniques for poststroke rehabilitation. Important results have been demonstrated, although they have not established the patients’ functional gain or related results of muscle electromyographic (EMG) data to functionality. Objective: The aim was to investigate EMG activity and sensory, motor, and functional performance in hemiparetic limbs of patients with stroke after intervention with MP and MT associated with conventional physical therapy training (CPTT). Methods: Seven patients were treated twice weekly during 8 weeks with MP and MT associated with CPTT of the affected upper limb. The Fugl-Meyer scale and the Barthel Index (BI) were applied to assess sensorimotor ability and independence of patients. Activation of the upper trapezius, biceps brachii, triceps brachii, flexor carpi ulnaris, and extensor carpi radialis was evaluated by means of EMG symmetry index and muscle co-activation measurements. Results: There were statistically significant differences between pre- and postassessment findings for the motor, sensory, and mobility domains of the Fugl-Meyer scale, as well as for BI evaluation. No statistically significant differences were observed when the pre- and posttest symmetry and co-activation data were compared, although there were qualitative changes. Conclusions: The protocol was effective for improving motor, sensory, and mobility aspects, as well as function involved in activities of daily living. Qualitative changes in symmetry and muscle co-contraction were found, indicating a possible improvement in upper limb rehabilitation of patients with stroke. Key words: electromyography, rehabilitation, stroke, upper limb extremity
troke is caused by the interruption of blood supply to the central nervous system, typically as a result of the rupture of a blood vessel or a blood clot.1 The most commonly compromised motor functions in individuals who have had a stroke occur in the upper limbs, involving the ability to reach, grip, and manipulate objects. These components form the basis of the motor skills required to successfully perform activities of daily living (ADLs).2,3 One of the deficiencies in the production of movement is caused by muscle weakness, which is attributed to improper recruitment of motor
S
units, leading to an inability to generate force.4 These deficits in muscle activation occur as a result of low neural conduction and less activation of the units in terms of firing rate and intraand intermuscular synchronization.5,6 Changes in motor units therefore lead to changes in the patterns of muscle activation, such as decreased ability to recruit agonist muscles, delayed onset of muscle activation, co-contraction of agonists and antagonists, and loss of selective activation of sets of muscles needed to perform motor tasks.7 In recent publications, researchers have described the use of mental practice (MP) and mirror therapy (MT)
Corresponding author: Rafael de A. Oliveira, Department of Physical Therapy, Federal University of Triangulo Mineiro, 405 Padre Zeferino Street, Uberaba, Minas Gerais, 38015-160 Brazil; e-mail: fael. [email protected]
Top Stroke Rehabil 2014;21(6):484–494 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com
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doi: 10.1310/tsr2106-484
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and their contribution to sensorimotor recovery after stroke.8-10 MP is defined as a dynamic state in which the individual mentally simulates a given action. With this technique, the individual feels himself or herself performing the imagined action. Such cognitive rehearsal of physical movements is able to activate, virtually, the same cortical areas that are activated during actual execution of the movements.11-13 The MT technique was introduced to the scientific community by Ramachandran and Rogers-Ramachandran14 with the aim of reducing phantom pain after upper limb amputation. This treatment modality is based on the image of the unaffected limb in front of a mirror, while the affected limb is behind the mirror. In this way, the visual feedback of the affected limb becomes the mirror image of the unaffected limb.8,9 The objective of MT is to combine motor stimulation with sensory feedback and to activate the premotor cortex, which has intimate connections with the areas involved in visual processing, thereby stimulating both the somatosensory and motor cortices of patients with stroke.8-10 With regard to these 2 types of intervention, most studies, including those that aimed at rehabilitation after stroke,11,12 have been directed toward understanding patterns of cortical activation.11,12,13,15,16 Few of the published studies have taken into account the possible changes in sensory and motor recovery, muscle activation, and functionality of patients undergoing these rehabilitation procedures. Hale,17 Harris and Robinson, 18 and Jowdy and Harris 19 used electromyographic (EMG) analysis to investigate and understand changes in muscles during the execution of MP by healthy individuals engaged in specific activities such as karate, juggling, and weight lifting. The EMG technique has been used to measure co-contraction and symmetry.20,21 However, there have been no studies in which EMG was used to measure the co-contraction of antagonist muscle pairs and symmetry after intervention with MP and MT in patients with stroke. The purpose of this study was to investigate the EMG activity and sensory, motor, and functional improvements in the upper limbs of patients with hemiparetic stroke after intervention with
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MP and MT in association with conventional physical therapy training (CPTT). Our hypothesis was that after following the protocol, the subjects would have better sensory, motor, and functional performance, as well as changes in activation of the paretic muscles during reaching functions. Methods This study can be described as a preliminary prospective intervention study, and it has been reviewed and approved by the Committee on Ethics in Research of the Federal University of Triângulo Mineiro (UFTM) (protocol number 1647). During the period from August 2012 to June 2013, in an open enrollment process, the patients were evaluated and treated at the Laboratory of Electromyography and Kinemetry (LAELCIN) of the Department of Applied Physical Therapy at UFTM. The first evaluation was conducted 2 days before the first therapy day, and the final evaluation was conducted on the second day after the end of the therapy period. After an explanation of the study was provided, all subjects signed consent forms to participate in this study. Patients at the Clinical Hospital of UFTM with a diagnosis of ischemic or hemorrhagic stroke were treated using the adapted protocol at the rehabilitation center linked to the hospital. The inclusion criteria used to select patients were as follows: (a) acute and subacute stroke phases (stroke 0.5 indicate greater activation of the BB muscle. When Equation 3 is used, values < 0.5 correspond to greater activation of the FCU muscle, and values > 0.5 correspond to greater activation of the ECR muscle.20
Si =
(Ai/A) Paretic (Ai/A) Healthy
Equation 1. Muscle Symmetry Calculation. A = area below the curve for a specific muscle; Ai = sum of the area below the curves for all muscles; Si = specific muscle symmetry.
Mental Practice and Mirror Therapy
Co-contraction TB/BB =
EMG biceps brachii (BB)
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× 100
EMG biceps brachii (BB) + EMG triceps brachii (TB) Equation 2. Adaptation of Hammond’s co-activation formula.32 EMG activity of TB/BB antagonist muscle pairs. Values greater than 0.5 indicate greater activation of the BB muscle.
Co-contraction (ERC/FUC) =
EMG extensor carpi radialis (ERC)
× 100
EMG extensor carpi radialis (ERC) + EMG flexor carpi ulnaris (FCU)
Equation 3. Adaptation of Hammond’s co-activation formula.32 EMG activity of ECR/FCU antagonist muscle pairs. Values greater than 0.5 indicate greater activation of the ECR muscle. Protocol
The practical implementation of MP and MT (adapted from the method of Moseley8) involved dividing the protocol into 3 treatment stages: (1) training of laterality (2 weeks), (2) imagination of hand movements (2 weeks), and (3) MT (4 weeks) (Table 1). The protocol was performed 2 times per week, with each session lasting 50 minutes. This included CPTT (15 minutes), upper limb functional training (adapted from the method of Gasparet al9) (10 minutes), and MP and MT (25 minutes) (Table 2). All treatment stages used functional training and imagined performance of functional positions. One physical therapist was responsible for examination of the patient, and 2 physiotherapists, one of whom was blinded to treatment, were responsible for the patient’s treatment. Data analysis
The data obtained for the patients were analyzed using descriptive statistics (mean and standard deviation). The Fugl-Meyer scale and BI values obeyed normality according to the Shapiro-Wilk test and were therefore analyzed using the t test for dependent samples, comparing the assessment results obtained before and after the trial. The muscle EMG activity data used for calculations of symmetry and co-contraction index were not normally distributed according to the same test. The EMG results were therefore analyzed by using
the Wilcoxon nonparametric test, also comparing the results from the initial and final assessments. A 5% significance level was used. Results The treatment protocol was applied to 7 patients (4 women and 3 men). The mean ± SD age was 56.3 ± 18.5 years, and the mean ± SD period since stroke was 4.14 ± 1.9 months. Only 1 patient was grade 1 on the Modified Ashworth Scale. The sample population is described in Table 3. In terms of the numbers of correct and incorrect answers during training of laterality, there were statistically significant differences between the success rates of the first and second sessions (t = -2.51, P = .04) and the first and fourth sessions (t = -3.51, P = .01). There were no statistically significant differences between the second and third sessions (t = -2.23, P = .07) or between the third and fourth sessions (t = -1.67, P = .14) (Figure 1). In analysis of the Fugl-Meyer scale results, the mean ± SD pre- and posttreatment values were as follows: 52 ± 8 and 62 ± 4 (motor), 21 ± 2 and 23 ± 1.5 (mobility), 10 ± 2 and 12 ± 0.5 (sensory), and 21 ± 2 and 23 ± 2 (pain). Statistically significant differences were found for the motor (Figure 2) (t = -4.82, P = .002), mobility (Figure 3) (t = 2.47, P = .05), and sensory (Figure 4) (t = -3.12, P = .02) domains. No difference was found for the pain domain (t = -1.90, P = .10). The pre- and posttreatment means ± SD for the BI were 65 ± 21 and 81 ± 12 points, respectively
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Table 1.
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Mental practice and mirror therapy protocol
Mental practice phases
Duration of each phase
Images
Phase description
1st stage: Training of laterality
2 weeks
42 images, with 21 left and 21 right, shown randomly
Patient is asked to identify the right and left hand for 5 seconds. The number of successes and failures is noted.
2nd stage: Imagination of hand movements
2 weeks
21 images of the affected hand, shown randomly
Patient is asked to imagine, 3 times, his/her hand in the position of the image shown.
3rd stage: Mirror therapy
4 weeks
21 images of the unaffected hand, shown randomly
Affected hand is within the mirror box, and unaffected hand is outside. Patient is asked to repeat the image movement with the unaffected hand, while simultaneously looking in the mirror and repeating the movement with the hand inside the mirror box.
Table 2.
Conventional physical therapy training (CPTT) and functional training
CPTT
Functional training
Performed only for the paretic side, with the patient sitting, with stretching held for 30 seconds and strengthening (3 sets of 10 repetitions each).
Performed with the unaffected hand outside the mirror box; the focus is on the reflection formed and repetition of the movements with the affected hand inside the mirror box (1 minute rest between activities).
Passive stretching of the muscles - Flexors of the fingers - Wrist flexors - Elbow flexors - Shoulder flexors - Internal rotators Strengthening the muscles - Extenders of the fingers - Handle extenders - Elbow extenders - Shoulder extenders - External rotators
Activities 1. Remove and replace balls in a glass. 2. Move a glass following the sequence marked on the mirror box, making the outline of a square. 3. Move a glass following the marking on the mirror box, performing an “X” movement. 4. Pick up and drop a ball, performing opponency with all fingers.
Table 3. Characteristics of research patients Characteristics Gender, F/M Age, years Dominant side, right/left Modified Ashworth Scale score (0/1/1+/2/3/4)
n or mean (±SD) 4/3 56.3 (±18.5) 7/0 6/1/0/0/0/0
Affected side, right/left)
4/3
Stroke type, (ischemic/hemorrhagic
7/0
Months after stroke
4.14 (±1.9)
MIQ-R score
81.3 (±11.3)
MMSE score
24.5 (±3)
Note: MIQ = revised movement imagery questionnaire; MMSE = Mini-Mental State Examination.
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(moderate dependence to mild dependence), and the differences were statistically significant (t = -5.64, P = .001) (Figure 5). Comparison of the pre- and postintervention symmetry values showed that there were no significant differences for the UT (t = 0.91, P = .40), BB (t = 1.014, P = .35), TB (t = 0.35, P = .74), FCU (t = -0.31, P = .77), and ECR (t = -1.13, P = .30) muscles. Qualitative analysis indicates that the contribution of the paretic ECR
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muscle increased from 0.82 (initial value) to 1.15 (postintervention). The opposite was found for the UT, BB, and TB muscles, with decreases from 1.16 to 1.07, 1.28 to 1.16, and 1.17 to 1.03, respectively (Table 4). There was no change in the symmetry value for the FCU muscle. Similarly, in the co-contraction analysis, the treatment caused no significant changes for the muscle pairs BB/TB [F(1, 24) = 0.54, P = .81] and FCU/ECR [F(1, 24) = 0.46, P = 0.50], and
40 35 30
Images answers
25 Corrects
20
Incorrects
15 10 5 0 1st Session 2nd Session 3rd Session 4th Session
Figure 1. Means and standard deviations of correct and incorrect answers during laterality training.
60
Fugl Meyer motor score
50
40
30
20
10
0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 2. Pre- and posttreatment motor evaluation using the Fugl-Meyer Scale. Mean and standard error (SE) of the patients’ score are presented.
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24 22 20
Fugl Meyer mobility score
18 16 14 12 10 8 6 4 2 0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 3. Pre- and posttreatment mobility evaluation using the Fugl-Meyer Scale. Mean and standard error (SE) of the patients’ scores are presented.
12
Fugl Meyer sensorial score
10
8
6
4
2
0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 4. Pre- and posttreatment sensory evaluation using the Fugl-Meyer scale. Mean and standard error (SE) of the patients’ scores are presented.
Mental Practice and Mirror Therapy
491
100
Barthel Index results
80
60
40
20
0
Barthel Pre-treatment
Barthel Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 5. Pre- and posttreatment Barthel Index results. Mean and standard error (SE) of the patients’ scores are presented.
no significant differences were observed between sides [BB/TB, F(1, 24) = 0.002, P = .96; FCU/ ECR, F(1, 24) = 0.46, P = .50]. Qualitative analysis Table 4. Pre- and posttreatment symmetry and co-contraction values Symmetry
Pretreatment
Posttreatment
UT
1.16
1.07
BB
1.28
1.16
TB
1.17
1.03
ECR
0.82
1.15
FCU
1.1
1.08
BB/TB
ECR/FCU
Affected side
0.3
0.41
Unaffected side
0.28
0.48
Unaffected side
0.3
0.48
Affected side
0.32
0.52
Co-contraction Pretreatment
Posttreatment
Note: Symmetry values for upper trapezius (UT), biceps brachii (BB), triceps brachii (TB), flexor carpi ulnaris (FCU), and extensor carpi radialis (ECR) and values of BB/TB and ECR/FCU antagonist pairs.
indicated that there were increased contributions of the TB and ECR muscles to performance of the movement (with values near or above 0.5), with the exception of the BB/TB pair of the unaffected side (Table 4). Discussion The hypothesis adopted in this study was that patients with poststroke hemiparesis would experience sensorimotor and independence improvements, as well as EMG changes, during activation of the upper limb muscles after treatment with MP and MT associated with CPTT. In agreement with findings of other studies,9,33,34 the results indicate significant improvements in sensorimotor performance and functional independence after treatment with this protocol. Although the changes in the EMG values for symmetry and muscle co-contraction were not statistically significant, there was qualitative improvement in the control of activation of the UT, TB, and ECR muscles. This study is the first to calculate the symmetry and co-contraction
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index values using EMG data for patients with hemiparesis after training with MP and MT. The Fugl-Meyer scale results were indicative of motor and mobility improvements. It has been reported that MP and repetitive use of the affected upper limb and the associated neural pathways can induce cortical changes.35 It is believed that MP can activate the areas involved in planning and controlling movements, such as the primary motor cortex, the superior parietal cortex, and the premotor area. 12,36 Other studies have also demonstrated cortical activation during MT training.15,16 In a recently published systematic review of 14 studies, investigators found significant motor, pain, and functional improvements in patients with stroke treated with MT.37 According to Shinoura et al,38 viewing the mirror reflection enables activation of the primary motor cortex of the ipsilateral injured hemisphere. Page et al36 also reported a relationship between brain activation and physical performance improvement after poststroke upper limb rehabilitation with MP treatment, indicated by changes in cerebral blood flow as determined by functional MRI and improvement in Fugl-Meyer scale scores. Significant improvements were found for the sensory domain of the Fugl-Meyer scale and in the number of correct image answers in the laterality training. An interesting finding was that in this study, the patients showed greater improvement during the first weeks of training. As the weeks elapsed, the patients continued to show laterality gains; however, the gains were greater for the first than for the last training session. This can be attributed to the correct right and left hand image information associated with the MT illusion that, in addition to motor cortex modulation and activation,38 may also influence activation of the occipital and somatosensory cortex.39 This should enable the patients to increase the sensory-discriminative ability of the visualized upper limb,7 hence contributing to sensory and laterality recovery. In association with MP and MT, this study also included conventional treatment of the affected upper limb (CPTT). This protocol was adopted because the exercises commonly used in conventional rehabilitation should help to maintain the musculoskeletal integrity of the affected limb during times when only the imagined ability
was stimulated. Butler and Page40 used a similar approach to investigate the motor and neural effects of MP with and without accompanying physical treatment and obtained results similar to those reported here. In the earlier study, 2 patients were treated with MP associated with conventional physical therapy: 1 patient received physical therapy only, and 1 patient received MP without physical therapy. The best improvement of performance in the Wolf Motor Function Test (WMFT) and in bilateral cortical activation was achieved for the patients who were treated with physical therapy together with MP. For the patient treated with MP alone, cortical activation was greater, but there was no significant motor effect. It is important to note that because of the combination of CPTT, MP, and MT, it is difficult to establish which specific factor (or set of factors) was responsible for the motor, sensory, and functional independence improvements presented by the patients. The EMG data for the muscles involved in the functional reach revealed no statistically significant difference between the pre- and posttreatment results. Nevertheless, it was possible to identify slight changes in the values of the symmetry and muscle co-contraction indices. According to the symmetry index, activation of the ECR muscle increased by 30% (from 0.82 to 1.15), indicating a greater contribution of the paretic muscle, which acted as an important stabilizer during movement implementation of the intervention protocol. For execution of the functional reach, the individual should not perform maximum muscle activation, but rather attempt to use greater motor control to achieve the desired goal, while the patterns of agonist and antagonist muscle activation are monitored during performance of the reach movement.41 Wagner et al42 analyzed the functional reach movement during acute and subacute poststroke rehabilitation and found that the deficit in the performance of the affected limb was probably due to a deficiency in agonist muscle activation, rather than excessive antagonist muscle activation. The results of this study, with qualitative changes in the EMG data and sensorimotor and functional improvement, therefore provide evidence for the effectiveness of the adopted protocol in increasing motor control, modifying the activation of the agonist muscles during the
Mental Practice and Mirror Therapy
movement according to the task. The findings also lend weight to the importance of task-oriented therapy following natural recovery after stroke,43 in which the stimulation related to specific ADLs seeks to shape muscle activation and the entire context of motor control involving the activity and its environmental context. The limitations of this study are the small number of patients evaluated and the short duration of the intervention. Because of the relevance of the topic, there is a need to perform more studies with larger samples and inclusion of control groups. This would assist in clarifying the sensorimotor and muscle activation changes that occur after implementation of the MP and MT protocol. Conclusion This study has demonstrated the effectiveness of the protocol in which MP and MT are used in
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association with conventional training for upper limb rehabilitation in patients with poststroke hemiparesis. There were improvements in the motor, sensory, and mobility Fugl-Meyer domains, as well as in functional performance during ADL. There were no statistically significant changes in the EMG values. However, qualitative changes were observed in the activation patterns related to symmetry and co-contraction of the TB and ECR muscles, indicating possible improvements in motor control. Acknowledgments The Research Support Foundation of Minas Gerais (FAPEMIG) provided a scholarship for Paula C. S. Vieira and Rafael de A. Oliveira. The authors thank the neurology research group at LAELCIN for contributing to the development of this research.
REFERENCES 1. World Health Organization. Stroke, cerebrovascular accident. 2013. http://www.who.int/topics/ cerebrovascular_accident/en/. Accessed March 18, 2013. 2. Cavaco NS, Alouche SR. Instrumentos de avaliação da função de membros superiores após acidente vascular encefálico: uma revisão sistemática. FisioterPesq. 2010;17(2):178-183. 3. Taub E, Uswatter G, Morris DM. Improved motor recovery after stroke and massive cortical reorganization following Constraint-Induced Movement Therapy. Phys Med Rehabil Clin N Am. 2003;14(1):S77–S91. 4. Gowland C, Debruin H, Basmanjian JV, Plews N, Brucea I. Agonist and antagonist activity during voluntary upper-limb movement in patients with stroke. Phys Ther. 1992; 2(9):624-633. 5. Barker RN, Brauer S, Carson R. Training-induced changes in the pattern of triceps to biceps activation during reaching tasks after chronic and severe stroke. Exp Brain Res. 2009;196:483-496. 6. Kamper DG, McKenna-Cole NA, Kahn LE, Reinkensmeyer, DJ. Alterations in reaching after stroke and their relation to movement direction and impairment severity. Arch Phys Med Rehabil. 2002;83(5):702-707. 7. Wagner JM, Dromerick AW, Sahrmann SA, Lang CE. Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol. 2007;118: 164-176. 8. Moseley G. Graded motor imagery is effective for long-standing complex regional pain
9.
10.
11.
12.
13. 14. 15.
16.
syndrome: A randomised controlled trial. Pain. 2004;108(1):192-198. Gaspar BE, Hotta TTH, Pascucci LA, de Souza S. Prática mental na reabilitação de membro superior após acidente vascular encefálico–casos clínicos. ConScientiae Saúde. 2011;10(2):319-325. Dohle C, Püllen J, Nakaten A, Küst J, Rietz C, Karbe H. Mirror therapy promotes recovery from severe hemiparesis: A randomized controlled trial. Neurorehabil Neural Repair. 2009;23(3):209217. Ietswaart M, Johnston M, Dijkerman HC, et al. Mental practice with motor imagery in stroke recovery: Randomized controlled trial of efficacy. Brain. 2011;134(5):1373-1386. Braun SM, Beurskens AJ, Borm PJ, Schack T, Wade DT. The effects of mental practice in stroke rehabilitation: A systematic review. Arch Phys Med Rehabil. 2006; 87(6):842-852. Decety J. The neurophysiological basis of motor imagery. Behav Brain Res. 1996;77(1):45-52. Ramachandran VS, Rogers-Ramachandran D. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. 1996;263(1369):377-386. Ezendam D, Bongers RM, Jannink MJ. Systematic review of the effectiveness of mirror therapy in upper extremity function. Disabil Rehabil. 2009;31(26):2135-2149. Toh SFM, Fong KNK. Systematic review on the effectiveness of mirror therapy in training upper limb hemiparesis after stroke. Hong Kong J Occup Ther. 2013;22(2):84-95.
494
TOPICS IN STROKE REHABILITATION/NOV-DEC 2014
17. Hale BD. The effects of internal and external imagery on muscular and ocular concomitants. J Sport Psychol. 1982;4:379-387. 18. Harris DV, Robinson WJ. The effects of skill level on EMG activity during internal and external imagery. J Sport Psychol. 1986;8:105-111. 19. Jowdy DP, Harris DV. Muscular responses during mental imagery as a function of motor skill level. J Sport Exercise Psychol. 1990;12:191-201. 20. Andrade R, Araújo R, Tucci H, Martins J, Oliveira A. Coactivation of the shoulder and arm muscles during closed kinetic chain exercises on an unstable surface. Singapore Med J. 2011; 52(1):35-41. 21. Kojović J, Miljković N, Janković MM, Popović DB. Recovery of motor function after stroke: A polymyography-based analysis. J Neurosci Methods. 2011;194(2):321-328. 22. Hall CR, Martin KA. Measuring movement imagery abilities: A revision of the Movement Imagery Questionnaire. J Mental Imagery. 1997;21(1-2):143-154. 23. Maki T, Quagliato E, Cacho E, et al. Estudo de confiabilidade da aplicação da escala de Fugl-Meyer no Brasil. Rev Bras Fisioter. 2006;10(2):177-183. 24. Gladstone DJ, Danells CJ, Black SE. The Fugl-Meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil Neural Repair. 2002;16(3):232-240. 25. Minosso JSM, Amendola F, Alvarenga MRM, Oliveira MDC. Validação, no Brasil, do Índice de Barthel em idosos atendidos em ambulatórios. Acta Paul Enferm. 2010;23(2):218-223. 26. Lees KR, Bath PMW, Schellinger PD, et al. Contemporary outcome measures in acute stroke research: Choice of primary outcome measure. Stroke. 2012;43(4):1163-1170. 27. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206-207. 28. Wu CY, Chen CL, Tang SF, Lin KC, Huang YY. Kinematic and clinical analyses of upperextremity movements after constraint-induced movement therapy in patients with stroke: A randomized controlled trial. Arch Phys Med Rehabil. 2007;88(8):964-970. 29. Thielman G, Kaminski T, Gentile A. Rehabilitation of reaching after stroke: Comparing 2 training protocols utilizing trunk restraint. Neurorehabil Neural Repair. 2008;22(6):697-705. 30. Raimundo KC, Silveira LS, Kishi MS, Fernandes L, Souza L. Análise cinemática e eletromiográfica do alcance em pacientes com acidente vascular encefálico. Fisioter Mov. 2011;24(1):87-97.
31. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10(5):361-374. 32. Hammond M, Fitts S, Kraft G, Nutter P, Trotter M, Robinson L. Co-contraction in the hemiparetic forearm: Quantitative EMG evaluation. Arch Phys Med Rehabil. 1988;69(5):348-351. 33. Liu KP, Chan CC, Lee TM, Hui-Chan CW. Mental imagery for promoting relearning for people after stroke: A randomized controlled trial. Arch Phys Med Rehabil. 2004;85(9):1403-1408. 34. Page SJ, Levine P, Sisto SA, Johnston MV. Mental practice combined with physical practice for upper-limb motor deficit in subacute stroke. Phys Ther. 2001;81(8):1455-1462. 35. Hewitt TE, Ford K, Levine P, Page SJ. Reaching kinematics to measure motor changes after mental practice in stroke. Top Stroke Rehabil. 2007;14(4):23-29. 36. Page SJ, Szaflarski JP, Eliassen JC, Pan H, Cramer SC. Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil Neural Repair. 2009;23(4):382-388. 37. Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror therapy for improving motor function after stroke. Stroke. 2013;44(1):e1-e2. 38. Shinoura N, Suzuki Y, Watanabe Y, et al. Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation. 2008;23(3):245-252. 39. Funase K, Tabira T, Higashi T, Liang N, Kasai T. Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett. 2007;419(2):108-112. 40. Butler AJ, Page SJ. Mental practice with motor imagery: Evidence for motor recovery and cortical reorganization after stroke. Arch Phys Med Rehabil. 2006;87(12):2-11. 41. Shumway-Cook A, Woollacott MH, de Lourdes Gianini M. Alcance, preensão e manipulação normais. In: Controle Motor: Teoria e Aplicações Práticas. São Paulo: Manole; 2003:427-448. 42. Wagner JM, Dromerick AW, Sahrmann SA, Lang CE. Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol. 2007;118(1): 164-176. 43. Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. Lancet. 2011;377(9778): 1693-1702.
Master's program in Physical Education, Federal University of Triângulo Mineiro (UFTM); 2Physiotherapist graduated from UFTM; 3 Department of Physical Therapy, UFTM, Uberaba, Minas Gerais, Brazil Background: The presence of sensory and motor deficits is common in patients post stroke. Mental practice (MP) and mirror therapy (MT) can be used as therapeutic techniques for poststroke rehabilitation. Important results have been demonstrated, although they have not established the patients’ functional gain or related results of muscle electromyographic (EMG) data to functionality. Objective: The aim was to investigate EMG activity and sensory, motor, and functional performance in hemiparetic limbs of patients with stroke after intervention with MP and MT associated with conventional physical therapy training (CPTT). Methods: Seven patients were treated twice weekly during 8 weeks with MP and MT associated with CPTT of the affected upper limb. The Fugl-Meyer scale and the Barthel Index (BI) were applied to assess sensorimotor ability and independence of patients. Activation of the upper trapezius, biceps brachii, triceps brachii, flexor carpi ulnaris, and extensor carpi radialis was evaluated by means of EMG symmetry index and muscle co-activation measurements. Results: There were statistically significant differences between pre- and postassessment findings for the motor, sensory, and mobility domains of the Fugl-Meyer scale, as well as for BI evaluation. No statistically significant differences were observed when the pre- and posttest symmetry and co-activation data were compared, although there were qualitative changes. Conclusions: The protocol was effective for improving motor, sensory, and mobility aspects, as well as function involved in activities of daily living. Qualitative changes in symmetry and muscle co-contraction were found, indicating a possible improvement in upper limb rehabilitation of patients with stroke. Key words: electromyography, rehabilitation, stroke, upper limb extremity
troke is caused by the interruption of blood supply to the central nervous system, typically as a result of the rupture of a blood vessel or a blood clot.1 The most commonly compromised motor functions in individuals who have had a stroke occur in the upper limbs, involving the ability to reach, grip, and manipulate objects. These components form the basis of the motor skills required to successfully perform activities of daily living (ADLs).2,3 One of the deficiencies in the production of movement is caused by muscle weakness, which is attributed to improper recruitment of motor
S
units, leading to an inability to generate force.4 These deficits in muscle activation occur as a result of low neural conduction and less activation of the units in terms of firing rate and intraand intermuscular synchronization.5,6 Changes in motor units therefore lead to changes in the patterns of muscle activation, such as decreased ability to recruit agonist muscles, delayed onset of muscle activation, co-contraction of agonists and antagonists, and loss of selective activation of sets of muscles needed to perform motor tasks.7 In recent publications, researchers have described the use of mental practice (MP) and mirror therapy (MT)
Corresponding author: Rafael de A. Oliveira, Department of Physical Therapy, Federal University of Triangulo Mineiro, 405 Padre Zeferino Street, Uberaba, Minas Gerais, 38015-160 Brazil; e-mail: fael. [email protected]
Top Stroke Rehabil 2014;21(6):484–494 © 2014 Thomas Land Publishers, Inc. www.strokejournal.com
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doi: 10.1310/tsr2106-484
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and their contribution to sensorimotor recovery after stroke.8-10 MP is defined as a dynamic state in which the individual mentally simulates a given action. With this technique, the individual feels himself or herself performing the imagined action. Such cognitive rehearsal of physical movements is able to activate, virtually, the same cortical areas that are activated during actual execution of the movements.11-13 The MT technique was introduced to the scientific community by Ramachandran and Rogers-Ramachandran14 with the aim of reducing phantom pain after upper limb amputation. This treatment modality is based on the image of the unaffected limb in front of a mirror, while the affected limb is behind the mirror. In this way, the visual feedback of the affected limb becomes the mirror image of the unaffected limb.8,9 The objective of MT is to combine motor stimulation with sensory feedback and to activate the premotor cortex, which has intimate connections with the areas involved in visual processing, thereby stimulating both the somatosensory and motor cortices of patients with stroke.8-10 With regard to these 2 types of intervention, most studies, including those that aimed at rehabilitation after stroke,11,12 have been directed toward understanding patterns of cortical activation.11,12,13,15,16 Few of the published studies have taken into account the possible changes in sensory and motor recovery, muscle activation, and functionality of patients undergoing these rehabilitation procedures. Hale,17 Harris and Robinson, 18 and Jowdy and Harris 19 used electromyographic (EMG) analysis to investigate and understand changes in muscles during the execution of MP by healthy individuals engaged in specific activities such as karate, juggling, and weight lifting. The EMG technique has been used to measure co-contraction and symmetry.20,21 However, there have been no studies in which EMG was used to measure the co-contraction of antagonist muscle pairs and symmetry after intervention with MP and MT in patients with stroke. The purpose of this study was to investigate the EMG activity and sensory, motor, and functional improvements in the upper limbs of patients with hemiparetic stroke after intervention with
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MP and MT in association with conventional physical therapy training (CPTT). Our hypothesis was that after following the protocol, the subjects would have better sensory, motor, and functional performance, as well as changes in activation of the paretic muscles during reaching functions. Methods This study can be described as a preliminary prospective intervention study, and it has been reviewed and approved by the Committee on Ethics in Research of the Federal University of Triângulo Mineiro (UFTM) (protocol number 1647). During the period from August 2012 to June 2013, in an open enrollment process, the patients were evaluated and treated at the Laboratory of Electromyography and Kinemetry (LAELCIN) of the Department of Applied Physical Therapy at UFTM. The first evaluation was conducted 2 days before the first therapy day, and the final evaluation was conducted on the second day after the end of the therapy period. After an explanation of the study was provided, all subjects signed consent forms to participate in this study. Patients at the Clinical Hospital of UFTM with a diagnosis of ischemic or hemorrhagic stroke were treated using the adapted protocol at the rehabilitation center linked to the hospital. The inclusion criteria used to select patients were as follows: (a) acute and subacute stroke phases (stroke 0.5 indicate greater activation of the BB muscle. When Equation 3 is used, values < 0.5 correspond to greater activation of the FCU muscle, and values > 0.5 correspond to greater activation of the ECR muscle.20
Si =
(Ai/A) Paretic (Ai/A) Healthy
Equation 1. Muscle Symmetry Calculation. A = area below the curve for a specific muscle; Ai = sum of the area below the curves for all muscles; Si = specific muscle symmetry.
Mental Practice and Mirror Therapy
Co-contraction TB/BB =
EMG biceps brachii (BB)
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× 100
EMG biceps brachii (BB) + EMG triceps brachii (TB) Equation 2. Adaptation of Hammond’s co-activation formula.32 EMG activity of TB/BB antagonist muscle pairs. Values greater than 0.5 indicate greater activation of the BB muscle.
Co-contraction (ERC/FUC) =
EMG extensor carpi radialis (ERC)
× 100
EMG extensor carpi radialis (ERC) + EMG flexor carpi ulnaris (FCU)
Equation 3. Adaptation of Hammond’s co-activation formula.32 EMG activity of ECR/FCU antagonist muscle pairs. Values greater than 0.5 indicate greater activation of the ECR muscle. Protocol
The practical implementation of MP and MT (adapted from the method of Moseley8) involved dividing the protocol into 3 treatment stages: (1) training of laterality (2 weeks), (2) imagination of hand movements (2 weeks), and (3) MT (4 weeks) (Table 1). The protocol was performed 2 times per week, with each session lasting 50 minutes. This included CPTT (15 minutes), upper limb functional training (adapted from the method of Gasparet al9) (10 minutes), and MP and MT (25 minutes) (Table 2). All treatment stages used functional training and imagined performance of functional positions. One physical therapist was responsible for examination of the patient, and 2 physiotherapists, one of whom was blinded to treatment, were responsible for the patient’s treatment. Data analysis
The data obtained for the patients were analyzed using descriptive statistics (mean and standard deviation). The Fugl-Meyer scale and BI values obeyed normality according to the Shapiro-Wilk test and were therefore analyzed using the t test for dependent samples, comparing the assessment results obtained before and after the trial. The muscle EMG activity data used for calculations of symmetry and co-contraction index were not normally distributed according to the same test. The EMG results were therefore analyzed by using
the Wilcoxon nonparametric test, also comparing the results from the initial and final assessments. A 5% significance level was used. Results The treatment protocol was applied to 7 patients (4 women and 3 men). The mean ± SD age was 56.3 ± 18.5 years, and the mean ± SD period since stroke was 4.14 ± 1.9 months. Only 1 patient was grade 1 on the Modified Ashworth Scale. The sample population is described in Table 3. In terms of the numbers of correct and incorrect answers during training of laterality, there were statistically significant differences between the success rates of the first and second sessions (t = -2.51, P = .04) and the first and fourth sessions (t = -3.51, P = .01). There were no statistically significant differences between the second and third sessions (t = -2.23, P = .07) or between the third and fourth sessions (t = -1.67, P = .14) (Figure 1). In analysis of the Fugl-Meyer scale results, the mean ± SD pre- and posttreatment values were as follows: 52 ± 8 and 62 ± 4 (motor), 21 ± 2 and 23 ± 1.5 (mobility), 10 ± 2 and 12 ± 0.5 (sensory), and 21 ± 2 and 23 ± 2 (pain). Statistically significant differences were found for the motor (Figure 2) (t = -4.82, P = .002), mobility (Figure 3) (t = 2.47, P = .05), and sensory (Figure 4) (t = -3.12, P = .02) domains. No difference was found for the pain domain (t = -1.90, P = .10). The pre- and posttreatment means ± SD for the BI were 65 ± 21 and 81 ± 12 points, respectively
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Table 1.
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Mental practice and mirror therapy protocol
Mental practice phases
Duration of each phase
Images
Phase description
1st stage: Training of laterality
2 weeks
42 images, with 21 left and 21 right, shown randomly
Patient is asked to identify the right and left hand for 5 seconds. The number of successes and failures is noted.
2nd stage: Imagination of hand movements
2 weeks
21 images of the affected hand, shown randomly
Patient is asked to imagine, 3 times, his/her hand in the position of the image shown.
3rd stage: Mirror therapy
4 weeks
21 images of the unaffected hand, shown randomly
Affected hand is within the mirror box, and unaffected hand is outside. Patient is asked to repeat the image movement with the unaffected hand, while simultaneously looking in the mirror and repeating the movement with the hand inside the mirror box.
Table 2.
Conventional physical therapy training (CPTT) and functional training
CPTT
Functional training
Performed only for the paretic side, with the patient sitting, with stretching held for 30 seconds and strengthening (3 sets of 10 repetitions each).
Performed with the unaffected hand outside the mirror box; the focus is on the reflection formed and repetition of the movements with the affected hand inside the mirror box (1 minute rest between activities).
Passive stretching of the muscles - Flexors of the fingers - Wrist flexors - Elbow flexors - Shoulder flexors - Internal rotators Strengthening the muscles - Extenders of the fingers - Handle extenders - Elbow extenders - Shoulder extenders - External rotators
Activities 1. Remove and replace balls in a glass. 2. Move a glass following the sequence marked on the mirror box, making the outline of a square. 3. Move a glass following the marking on the mirror box, performing an “X” movement. 4. Pick up and drop a ball, performing opponency with all fingers.
Table 3. Characteristics of research patients Characteristics Gender, F/M Age, years Dominant side, right/left Modified Ashworth Scale score (0/1/1+/2/3/4)
n or mean (±SD) 4/3 56.3 (±18.5) 7/0 6/1/0/0/0/0
Affected side, right/left)
4/3
Stroke type, (ischemic/hemorrhagic
7/0
Months after stroke
4.14 (±1.9)
MIQ-R score
81.3 (±11.3)
MMSE score
24.5 (±3)
Note: MIQ = revised movement imagery questionnaire; MMSE = Mini-Mental State Examination.
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(moderate dependence to mild dependence), and the differences were statistically significant (t = -5.64, P = .001) (Figure 5). Comparison of the pre- and postintervention symmetry values showed that there were no significant differences for the UT (t = 0.91, P = .40), BB (t = 1.014, P = .35), TB (t = 0.35, P = .74), FCU (t = -0.31, P = .77), and ECR (t = -1.13, P = .30) muscles. Qualitative analysis indicates that the contribution of the paretic ECR
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muscle increased from 0.82 (initial value) to 1.15 (postintervention). The opposite was found for the UT, BB, and TB muscles, with decreases from 1.16 to 1.07, 1.28 to 1.16, and 1.17 to 1.03, respectively (Table 4). There was no change in the symmetry value for the FCU muscle. Similarly, in the co-contraction analysis, the treatment caused no significant changes for the muscle pairs BB/TB [F(1, 24) = 0.54, P = .81] and FCU/ECR [F(1, 24) = 0.46, P = 0.50], and
40 35 30
Images answers
25 Corrects
20
Incorrects
15 10 5 0 1st Session 2nd Session 3rd Session 4th Session
Figure 1. Means and standard deviations of correct and incorrect answers during laterality training.
60
Fugl Meyer motor score
50
40
30
20
10
0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 2. Pre- and posttreatment motor evaluation using the Fugl-Meyer Scale. Mean and standard error (SE) of the patients’ score are presented.
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24 22 20
Fugl Meyer mobility score
18 16 14 12 10 8 6 4 2 0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 3. Pre- and posttreatment mobility evaluation using the Fugl-Meyer Scale. Mean and standard error (SE) of the patients’ scores are presented.
12
Fugl Meyer sensorial score
10
8
6
4
2
0 Fugl Pre-treatment
Fugl Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 4. Pre- and posttreatment sensory evaluation using the Fugl-Meyer scale. Mean and standard error (SE) of the patients’ scores are presented.
Mental Practice and Mirror Therapy
491
100
Barthel Index results
80
60
40
20
0
Barthel Pre-treatment
Barthel Post-treatment
Mean Mean±SE Mean±1,96*SE
Figure 5. Pre- and posttreatment Barthel Index results. Mean and standard error (SE) of the patients’ scores are presented.
no significant differences were observed between sides [BB/TB, F(1, 24) = 0.002, P = .96; FCU/ ECR, F(1, 24) = 0.46, P = .50]. Qualitative analysis Table 4. Pre- and posttreatment symmetry and co-contraction values Symmetry
Pretreatment
Posttreatment
UT
1.16
1.07
BB
1.28
1.16
TB
1.17
1.03
ECR
0.82
1.15
FCU
1.1
1.08
BB/TB
ECR/FCU
Affected side
0.3
0.41
Unaffected side
0.28
0.48
Unaffected side
0.3
0.48
Affected side
0.32
0.52
Co-contraction Pretreatment
Posttreatment
Note: Symmetry values for upper trapezius (UT), biceps brachii (BB), triceps brachii (TB), flexor carpi ulnaris (FCU), and extensor carpi radialis (ECR) and values of BB/TB and ECR/FCU antagonist pairs.
indicated that there were increased contributions of the TB and ECR muscles to performance of the movement (with values near or above 0.5), with the exception of the BB/TB pair of the unaffected side (Table 4). Discussion The hypothesis adopted in this study was that patients with poststroke hemiparesis would experience sensorimotor and independence improvements, as well as EMG changes, during activation of the upper limb muscles after treatment with MP and MT associated with CPTT. In agreement with findings of other studies,9,33,34 the results indicate significant improvements in sensorimotor performance and functional independence after treatment with this protocol. Although the changes in the EMG values for symmetry and muscle co-contraction were not statistically significant, there was qualitative improvement in the control of activation of the UT, TB, and ECR muscles. This study is the first to calculate the symmetry and co-contraction
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index values using EMG data for patients with hemiparesis after training with MP and MT. The Fugl-Meyer scale results were indicative of motor and mobility improvements. It has been reported that MP and repetitive use of the affected upper limb and the associated neural pathways can induce cortical changes.35 It is believed that MP can activate the areas involved in planning and controlling movements, such as the primary motor cortex, the superior parietal cortex, and the premotor area. 12,36 Other studies have also demonstrated cortical activation during MT training.15,16 In a recently published systematic review of 14 studies, investigators found significant motor, pain, and functional improvements in patients with stroke treated with MT.37 According to Shinoura et al,38 viewing the mirror reflection enables activation of the primary motor cortex of the ipsilateral injured hemisphere. Page et al36 also reported a relationship between brain activation and physical performance improvement after poststroke upper limb rehabilitation with MP treatment, indicated by changes in cerebral blood flow as determined by functional MRI and improvement in Fugl-Meyer scale scores. Significant improvements were found for the sensory domain of the Fugl-Meyer scale and in the number of correct image answers in the laterality training. An interesting finding was that in this study, the patients showed greater improvement during the first weeks of training. As the weeks elapsed, the patients continued to show laterality gains; however, the gains were greater for the first than for the last training session. This can be attributed to the correct right and left hand image information associated with the MT illusion that, in addition to motor cortex modulation and activation,38 may also influence activation of the occipital and somatosensory cortex.39 This should enable the patients to increase the sensory-discriminative ability of the visualized upper limb,7 hence contributing to sensory and laterality recovery. In association with MP and MT, this study also included conventional treatment of the affected upper limb (CPTT). This protocol was adopted because the exercises commonly used in conventional rehabilitation should help to maintain the musculoskeletal integrity of the affected limb during times when only the imagined ability
was stimulated. Butler and Page40 used a similar approach to investigate the motor and neural effects of MP with and without accompanying physical treatment and obtained results similar to those reported here. In the earlier study, 2 patients were treated with MP associated with conventional physical therapy: 1 patient received physical therapy only, and 1 patient received MP without physical therapy. The best improvement of performance in the Wolf Motor Function Test (WMFT) and in bilateral cortical activation was achieved for the patients who were treated with physical therapy together with MP. For the patient treated with MP alone, cortical activation was greater, but there was no significant motor effect. It is important to note that because of the combination of CPTT, MP, and MT, it is difficult to establish which specific factor (or set of factors) was responsible for the motor, sensory, and functional independence improvements presented by the patients. The EMG data for the muscles involved in the functional reach revealed no statistically significant difference between the pre- and posttreatment results. Nevertheless, it was possible to identify slight changes in the values of the symmetry and muscle co-contraction indices. According to the symmetry index, activation of the ECR muscle increased by 30% (from 0.82 to 1.15), indicating a greater contribution of the paretic muscle, which acted as an important stabilizer during movement implementation of the intervention protocol. For execution of the functional reach, the individual should not perform maximum muscle activation, but rather attempt to use greater motor control to achieve the desired goal, while the patterns of agonist and antagonist muscle activation are monitored during performance of the reach movement.41 Wagner et al42 analyzed the functional reach movement during acute and subacute poststroke rehabilitation and found that the deficit in the performance of the affected limb was probably due to a deficiency in agonist muscle activation, rather than excessive antagonist muscle activation. The results of this study, with qualitative changes in the EMG data and sensorimotor and functional improvement, therefore provide evidence for the effectiveness of the adopted protocol in increasing motor control, modifying the activation of the agonist muscles during the
Mental Practice and Mirror Therapy
movement according to the task. The findings also lend weight to the importance of task-oriented therapy following natural recovery after stroke,43 in which the stimulation related to specific ADLs seeks to shape muscle activation and the entire context of motor control involving the activity and its environmental context. The limitations of this study are the small number of patients evaluated and the short duration of the intervention. Because of the relevance of the topic, there is a need to perform more studies with larger samples and inclusion of control groups. This would assist in clarifying the sensorimotor and muscle activation changes that occur after implementation of the MP and MT protocol. Conclusion This study has demonstrated the effectiveness of the protocol in which MP and MT are used in
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association with conventional training for upper limb rehabilitation in patients with poststroke hemiparesis. There were improvements in the motor, sensory, and mobility Fugl-Meyer domains, as well as in functional performance during ADL. There were no statistically significant changes in the EMG values. However, qualitative changes were observed in the activation patterns related to symmetry and co-contraction of the TB and ECR muscles, indicating possible improvements in motor control. Acknowledgments The Research Support Foundation of Minas Gerais (FAPEMIG) provided a scholarship for Paula C. S. Vieira and Rafael de A. Oliveira. The authors thank the neurology research group at LAELCIN for contributing to the development of this research.
REFERENCES 1. World Health Organization. Stroke, cerebrovascular accident. 2013. http://www.who.int/topics/ cerebrovascular_accident/en/. Accessed March 18, 2013. 2. Cavaco NS, Alouche SR. Instrumentos de avaliação da função de membros superiores após acidente vascular encefálico: uma revisão sistemática. FisioterPesq. 2010;17(2):178-183. 3. Taub E, Uswatter G, Morris DM. Improved motor recovery after stroke and massive cortical reorganization following Constraint-Induced Movement Therapy. Phys Med Rehabil Clin N Am. 2003;14(1):S77–S91. 4. Gowland C, Debruin H, Basmanjian JV, Plews N, Brucea I. Agonist and antagonist activity during voluntary upper-limb movement in patients with stroke. Phys Ther. 1992; 2(9):624-633. 5. Barker RN, Brauer S, Carson R. Training-induced changes in the pattern of triceps to biceps activation during reaching tasks after chronic and severe stroke. Exp Brain Res. 2009;196:483-496. 6. Kamper DG, McKenna-Cole NA, Kahn LE, Reinkensmeyer, DJ. Alterations in reaching after stroke and their relation to movement direction and impairment severity. Arch Phys Med Rehabil. 2002;83(5):702-707. 7. Wagner JM, Dromerick AW, Sahrmann SA, Lang CE. Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol. 2007;118: 164-176. 8. Moseley G. Graded motor imagery is effective for long-standing complex regional pain
9.
10.
11.
12.
13. 14. 15.
16.
syndrome: A randomised controlled trial. Pain. 2004;108(1):192-198. Gaspar BE, Hotta TTH, Pascucci LA, de Souza S. Prática mental na reabilitação de membro superior após acidente vascular encefálico–casos clínicos. ConScientiae Saúde. 2011;10(2):319-325. Dohle C, Püllen J, Nakaten A, Küst J, Rietz C, Karbe H. Mirror therapy promotes recovery from severe hemiparesis: A randomized controlled trial. Neurorehabil Neural Repair. 2009;23(3):209217. Ietswaart M, Johnston M, Dijkerman HC, et al. Mental practice with motor imagery in stroke recovery: Randomized controlled trial of efficacy. Brain. 2011;134(5):1373-1386. Braun SM, Beurskens AJ, Borm PJ, Schack T, Wade DT. The effects of mental practice in stroke rehabilitation: A systematic review. Arch Phys Med Rehabil. 2006; 87(6):842-852. Decety J. The neurophysiological basis of motor imagery. Behav Brain Res. 1996;77(1):45-52. Ramachandran VS, Rogers-Ramachandran D. Synaesthesia in phantom limbs induced with mirrors. Proc Biol Sci. 1996;263(1369):377-386. Ezendam D, Bongers RM, Jannink MJ. Systematic review of the effectiveness of mirror therapy in upper extremity function. Disabil Rehabil. 2009;31(26):2135-2149. Toh SFM, Fong KNK. Systematic review on the effectiveness of mirror therapy in training upper limb hemiparesis after stroke. Hong Kong J Occup Ther. 2013;22(2):84-95.
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17. Hale BD. The effects of internal and external imagery on muscular and ocular concomitants. J Sport Psychol. 1982;4:379-387. 18. Harris DV, Robinson WJ. The effects of skill level on EMG activity during internal and external imagery. J Sport Psychol. 1986;8:105-111. 19. Jowdy DP, Harris DV. Muscular responses during mental imagery as a function of motor skill level. J Sport Exercise Psychol. 1990;12:191-201. 20. Andrade R, Araújo R, Tucci H, Martins J, Oliveira A. Coactivation of the shoulder and arm muscles during closed kinetic chain exercises on an unstable surface. Singapore Med J. 2011; 52(1):35-41. 21. Kojović J, Miljković N, Janković MM, Popović DB. Recovery of motor function after stroke: A polymyography-based analysis. J Neurosci Methods. 2011;194(2):321-328. 22. Hall CR, Martin KA. Measuring movement imagery abilities: A revision of the Movement Imagery Questionnaire. J Mental Imagery. 1997;21(1-2):143-154. 23. Maki T, Quagliato E, Cacho E, et al. Estudo de confiabilidade da aplicação da escala de Fugl-Meyer no Brasil. Rev Bras Fisioter. 2006;10(2):177-183. 24. Gladstone DJ, Danells CJ, Black SE. The Fugl-Meyer assessment of motor recovery after stroke: A critical review of its measurement properties. Neurorehabil Neural Repair. 2002;16(3):232-240. 25. Minosso JSM, Amendola F, Alvarenga MRM, Oliveira MDC. Validação, no Brasil, do Índice de Barthel em idosos atendidos em ambulatórios. Acta Paul Enferm. 2010;23(2):218-223. 26. Lees KR, Bath PMW, Schellinger PD, et al. Contemporary outcome measures in acute stroke research: Choice of primary outcome measure. Stroke. 2012;43(4):1163-1170. 27. Bohannon RW, Smith MB. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther. 1987;67(2):206-207. 28. Wu CY, Chen CL, Tang SF, Lin KC, Huang YY. Kinematic and clinical analyses of upperextremity movements after constraint-induced movement therapy in patients with stroke: A randomized controlled trial. Arch Phys Med Rehabil. 2007;88(8):964-970. 29. Thielman G, Kaminski T, Gentile A. Rehabilitation of reaching after stroke: Comparing 2 training protocols utilizing trunk restraint. Neurorehabil Neural Repair. 2008;22(6):697-705. 30. Raimundo KC, Silveira LS, Kishi MS, Fernandes L, Souza L. Análise cinemática e eletromiográfica do alcance em pacientes com acidente vascular encefálico. Fisioter Mov. 2011;24(1):87-97.
31. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G. Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol. 2000;10(5):361-374. 32. Hammond M, Fitts S, Kraft G, Nutter P, Trotter M, Robinson L. Co-contraction in the hemiparetic forearm: Quantitative EMG evaluation. Arch Phys Med Rehabil. 1988;69(5):348-351. 33. Liu KP, Chan CC, Lee TM, Hui-Chan CW. Mental imagery for promoting relearning for people after stroke: A randomized controlled trial. Arch Phys Med Rehabil. 2004;85(9):1403-1408. 34. Page SJ, Levine P, Sisto SA, Johnston MV. Mental practice combined with physical practice for upper-limb motor deficit in subacute stroke. Phys Ther. 2001;81(8):1455-1462. 35. Hewitt TE, Ford K, Levine P, Page SJ. Reaching kinematics to measure motor changes after mental practice in stroke. Top Stroke Rehabil. 2007;14(4):23-29. 36. Page SJ, Szaflarski JP, Eliassen JC, Pan H, Cramer SC. Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil Neural Repair. 2009;23(4):382-388. 37. Thieme H, Mehrholz J, Pohl M, Behrens J, Dohle C. Mirror therapy for improving motor function after stroke. Stroke. 2013;44(1):e1-e2. 38. Shinoura N, Suzuki Y, Watanabe Y, et al. Mirror therapy activates outside of cerebellum and ipsilateral M1. NeuroRehabilitation. 2008;23(3):245-252. 39. Funase K, Tabira T, Higashi T, Liang N, Kasai T. Increased corticospinal excitability during direct observation of self-movement and indirect observation with a mirror box. Neurosci Lett. 2007;419(2):108-112. 40. Butler AJ, Page SJ. Mental practice with motor imagery: Evidence for motor recovery and cortical reorganization after stroke. Arch Phys Med Rehabil. 2006;87(12):2-11. 41. Shumway-Cook A, Woollacott MH, de Lourdes Gianini M. Alcance, preensão e manipulação normais. In: Controle Motor: Teoria e Aplicações Práticas. São Paulo: Manole; 2003:427-448. 42. Wagner JM, Dromerick AW, Sahrmann SA, Lang CE. Upper extremity muscle activation during recovery of reaching in subjects with post-stroke hemiparesis. Clin Neurophysiol. 2007;118(1): 164-176. 43. Langhorne P, Bernhardt J, Kwakkel G. Stroke rehabilitation. Lancet. 2011;377(9778): 1693-1702.
