Original Paper Received: September 18, 2013 Accepted: November 19, 2013 Published online: January 16, 2014
Cerebrovasc Dis 2014;37:123–127 DOI: 10.1159/000357421
Immediate Effects of Unaffected Arm Exercise in Poststroke Patients with Spastic Upper Limb Hemiparesis Keiko Sakamoto a Takeshi Nakamura b Hiroyasu Uenishi b Yasunori Umemoto a Hideki Arakawa a Masahiro Abo d Ryuichi Saura c Hiroyoshi Fujiwara e Toshikazu Kubo e Fumihiro Tajima b
a
Research Center of Sports Medicine and Balneology and b Department of Rehabilitation Medicine, Wakayama Medical University, Wakayama, c Department of Rehabilitation Medicine, Division of Comprehensive Medicine, Osaka Medical Collage, Osaka, d Department of Rehabilitation Medicine, Jikei University School of Medicine, Tokyo, and e Department of Orthopaedics, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Japan
Key Words Stroke · Spasticity · Unaffected arm exercise
Abstract Background: Spasticity is a major disabling symptom in stroke patients. Clinically, one of the goals of management of stroke patients should be to reduce spasticity. Recent evidence suggests that motor recovery after stroke comprises a hierarchical, dynamic framework of interacting mechanisms in brain cortex. We hypothesized that unaffected arm exercise can stimulate the ipsilateral motor cortex and change the affected upper limb function and spasticity in stroke patients. To test the hypothesis, we evaluated the effects of unaffected arm exercise on spasticity of the affected upper limb and motor function in stroke patients. Methods: The study was performed in 41 chronic stroke patients with upper limb hemiparesis. Affected upper limb spasticity and function were assessed at baseline and after each intervention by the modified Ashworth Scale and Fugl-Meyer Assessment, respectively. Patients were also evaluated clinically by
© 2014 S. Karger AG, Basel 1015–9770/14/0372–0123$39.50/0 E-Mail [email protected] www.karger.com/ced
the modified Rankin Scale, Functional Independence Measurement and National Institutes of Health Stroke Scale. Subjects stood for 10 min during the control period, and then cycled an arm crank ergometer at 50% of maximum work load for 10 min by the unaffected arm in standing position. Results: The mean age at study entry was 64.6 ± 1.7 years. The latency between onset of stroke and the study was 109.0 ± 17.0 months (range, 6–495). The cause of hemiparesis was cerebral infarction (n = 21), intracerebral hemorrhage (n = 17) or subarachnoid hemorrhage (n = 3). Exercise significantly improved the modified Ashworth Scale compared with baseline (p < 0.0001). No such change was noted after the control intervention. The Fugl-Meyer Assessment score did not change after exercise compared with baseline (p = 0.95). Conclusions: We conclude that 10 min of unaffected arm exercise improves the affected upper limb spasticity in stroke patients. Further studies are needed to determine the exact mechanism of such improvement and the long-term effects of unaffected arm exercise on motor performance. © 2014 S. Karger AG, Basel
Takeshi Nakamura, MD, PhD Department of Rehabilitation Medicine Wakayama Medical University 811-1, Kimiidera, Wakayama City, Wakayama 641-8509 (Japan) E-Mail take-n @ wakayama-med.ac.jp
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Poststroke spasticity (PSS) is a common complication associated with other signs and symptoms of upper motor neuron syndrome, including agonist/antagonist cocontraction, weakness and lack of coordination. The definition of spasticity is ‘motor disorder characterized by a velocity-dependent increase in muscle tone and tonic stretch reflexes with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome’ [1, 2]. PSS contributes to impairments and disabilities that negatively impact functional recovery and result in gait abnormalities and problems with arm use. Therefore, PSS may lead to reduced quality of life, increased pain and joint contractures. Clinically, one of the goals of management of PSS should be to reduce muscle hypertonia. Currently available therapeutic interventions for spasticity are based on peripheral strategies (e.g. physical techniques to increase muscle length through stretching, pharmacological and surgical interventions) as well as central strategies. With regard to the latter, only a limited number of effective rehabilitation techniques to reduce spasticity per se are available at present. Recent evidence suggests that motor recovery after stroke comprises a hierarchical, dynamic framework of interacting mechanisms [3, 4]. Usually after the loss of interhemispheric inhibition from the ipsilesional motor cortex to the contralesional hemisphere following stroke, there is a tendency for overactivity to begin in the contralesional hemisphere soon after the stroke [5, 6]. In the chronic stage, the resulting transcallosal imbalance might hinder cortical reorganization within the ipsilesional hemisphere. This is considered to be a predictor for poor recovery from brain insult [4]. Although its efficacy is still under consideration, repetitive transcranial magnetic stimulation (rTMS) has been used to modulate cortical excitability and harness neuroplasticity in stroke patients to promote motor recovery [7– 12]. High-frequency rTMS facilitates cortical excitability [7, 8], whereas low-frequency rTMS decreases cortical excitability of the stimulated hemisphere [9, 10] and increases cortical excitability of the nonstimulated hemisphere [11, 12]. Thus, the loss of normal interhemispheric inhibition of movement-related brain activation impairs performance by reducing the selectivity of motor unit activation in stroke patients [13]. Therefore, low-frequency rTMS suppresses cortical hyperexcitability in the unaffected hemisphere while high-frequency rTMS activates depressed cortical areas in the 124
Cerebrovasc Dis 2014;37:123–127 DOI: 10.1159/000357421
affected hemisphere, rebalances the interhemispheric inhibition, and corrects impaired performance. In this regard, evidence suggests that hand motor tasks can activate the ipsilateral motor cortex [14]. Moreover, Woldag et al. [15] showed that voluntary activation of the unaffected hand excited the affected hemisphere in stroke patients. The hypothesis tested in this multicenter pilot study was that unaffected arm exercise can activate or inhibit the effects of contralesional motor cortical area and change the function and spasticity of the affected upper limb in stroke patients. To test the hypothesis, we assessed the effects of unaffected arm exercise on upper limb spasticity and function in stroke patients. Materials and Methods Participants A total of 41 consecutive patients with stroke participated in the study. All patients presented with upper limb hemiparesis. Before the onset of stroke, none of the subjects had any medical motorrelated problems due to bone and joint disorders or neurological problems. All subjects had retired from their jobs after the stroke. The inclusion criteria were as follows: (1) history of cerebrovascular accident of at least 6 months, (2) stroke-related paralysis of the upper extremity associated with neuromuscular dysfunction and (3) signing an informed consent based on the institutional ethics review board procedures. Subjects were excluded for the following reasons: (1) if they were medically unstable (e.g. unstable cardiovascular status) and (2) if they suffered significant musculoskeletal problems apart from those related to stroke. For those who were previously admitted to local hospitals, the medical records were obtained to confirm the diagnosis of stroke based on imaging findings (e.g. CT scan and MRI). In addition, the primary care physician was also required to complete a form to confirm the diagnosis of stroke and provide relevant medical history of the subjects (e.g. characteristics of stroke, contraindications to exercise, comorbid conditions). The study procedures were approved by the ethics committee of Wakayama Medical University and adhered to the Declaration of Helsinki. All participants gave written consent before participating in the study. Evaluation of Clinical Status The Functional Independence Measurement [16] was used to describe the functional status on 18 standardized items. The clinical status of each patient was also assessed using the modified Rankin Scale [17] and the National Institutes of Health Stroke Scale [18]. Control and Exercise Intervention Protocol Before the scheduled start of the study, each subject underwent measurement of the maximum work load on an arm crank ergometer (881E Hand Ergometer; Monark, Sweden) using the arm unaffected by stroke while in standing position. The test end point was inability to maintain a cycling cadence of at least 40 rpm [19]. Following an initial rest period of approximately 10 min (baseline),
Sakamoto et al.
Downloaded by: Selçuk Universitesi 193.255.248.150 - 1/29/2015 4:03:52 AM
Introduction
the subject stood for 10 min (control intervention). For exercise, following adequate rest, the subject began cycling an arm crank ergometer at 50% of maximum workload for 10 min using the unaffected arm in standing position. The workload was kept constant in all subjects. The subject maintained a target cadence of 60 rpm throughout the exercise. Baseline and Postintervention Evaluation All subjects underwent blinded evaluation using the modified Ashworth Scale and upper extremity Fugl-Meyer Assessment by a physical therapist who provided the patient with no training to ensure bias-free outcome evaluation. At baseline and after each intervention, the affected arm was physically examined with the modified Ashworth Scale and Fugl-Meyer Assessment. The modified Ashworth Scale grades muscle tone from 0 to 5, with 0 for no increase in muscle tone to 5 for a rigid joint [20]. We used the modified Ashworth Scale to assess spasticity of shoulder adductors, elbow flexors, wrist flexors and finger flexors in the paretic upper extremity. We also used the Fugl-Meyer Assessment to evaluate the severity of motor impairment in the paretic upper extremity [21]. This examination is based on the performance of 33 tasks, which assess the quality of movements, reflex activity and coordination. A score based on a 3-point ordinal scale (0–2) was given to each task, with a higher score indicating less impairment (maximum score, 66). The Fugl-Meyer Assessment is reported to have high interrater reliability (r = 0.99) [22]. Statistical Analysis Data were expressed as mean ± SEM. To facilitate data analysis, the modified Ashworth Scale scores 0, 1, 1+, 2, 3, and 4 were assigned numerical values designated as 0, 1, 2, 3, 4, and 5, respectively. Differences between data recorded at baseline and each intervention were analyzed by ANOVA followed by Scheffe’s F test. A p value
Cerebrovasc Dis 2014;37:123–127 DOI: 10.1159/000357421
Immediate Effects of Unaffected Arm Exercise in Poststroke Patients with Spastic Upper Limb Hemiparesis Keiko Sakamoto a Takeshi Nakamura b Hiroyasu Uenishi b Yasunori Umemoto a Hideki Arakawa a Masahiro Abo d Ryuichi Saura c Hiroyoshi Fujiwara e Toshikazu Kubo e Fumihiro Tajima b
a
Research Center of Sports Medicine and Balneology and b Department of Rehabilitation Medicine, Wakayama Medical University, Wakayama, c Department of Rehabilitation Medicine, Division of Comprehensive Medicine, Osaka Medical Collage, Osaka, d Department of Rehabilitation Medicine, Jikei University School of Medicine, Tokyo, and e Department of Orthopaedics, Graduate School of Medical Science, Kyoto Prefectural University of Medicine, Kyoto, Japan
Key Words Stroke · Spasticity · Unaffected arm exercise
Abstract Background: Spasticity is a major disabling symptom in stroke patients. Clinically, one of the goals of management of stroke patients should be to reduce spasticity. Recent evidence suggests that motor recovery after stroke comprises a hierarchical, dynamic framework of interacting mechanisms in brain cortex. We hypothesized that unaffected arm exercise can stimulate the ipsilateral motor cortex and change the affected upper limb function and spasticity in stroke patients. To test the hypothesis, we evaluated the effects of unaffected arm exercise on spasticity of the affected upper limb and motor function in stroke patients. Methods: The study was performed in 41 chronic stroke patients with upper limb hemiparesis. Affected upper limb spasticity and function were assessed at baseline and after each intervention by the modified Ashworth Scale and Fugl-Meyer Assessment, respectively. Patients were also evaluated clinically by
© 2014 S. Karger AG, Basel 1015–9770/14/0372–0123$39.50/0 E-Mail [email protected] www.karger.com/ced
the modified Rankin Scale, Functional Independence Measurement and National Institutes of Health Stroke Scale. Subjects stood for 10 min during the control period, and then cycled an arm crank ergometer at 50% of maximum work load for 10 min by the unaffected arm in standing position. Results: The mean age at study entry was 64.6 ± 1.7 years. The latency between onset of stroke and the study was 109.0 ± 17.0 months (range, 6–495). The cause of hemiparesis was cerebral infarction (n = 21), intracerebral hemorrhage (n = 17) or subarachnoid hemorrhage (n = 3). Exercise significantly improved the modified Ashworth Scale compared with baseline (p < 0.0001). No such change was noted after the control intervention. The Fugl-Meyer Assessment score did not change after exercise compared with baseline (p = 0.95). Conclusions: We conclude that 10 min of unaffected arm exercise improves the affected upper limb spasticity in stroke patients. Further studies are needed to determine the exact mechanism of such improvement and the long-term effects of unaffected arm exercise on motor performance. © 2014 S. Karger AG, Basel
Takeshi Nakamura, MD, PhD Department of Rehabilitation Medicine Wakayama Medical University 811-1, Kimiidera, Wakayama City, Wakayama 641-8509 (Japan) E-Mail take-n @ wakayama-med.ac.jp
Downloaded by: Selçuk Universitesi 193.255.248.150 - 1/29/2015 4:03:52 AM
Poststroke spasticity (PSS) is a common complication associated with other signs and symptoms of upper motor neuron syndrome, including agonist/antagonist cocontraction, weakness and lack of coordination. The definition of spasticity is ‘motor disorder characterized by a velocity-dependent increase in muscle tone and tonic stretch reflexes with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome’ [1, 2]. PSS contributes to impairments and disabilities that negatively impact functional recovery and result in gait abnormalities and problems with arm use. Therefore, PSS may lead to reduced quality of life, increased pain and joint contractures. Clinically, one of the goals of management of PSS should be to reduce muscle hypertonia. Currently available therapeutic interventions for spasticity are based on peripheral strategies (e.g. physical techniques to increase muscle length through stretching, pharmacological and surgical interventions) as well as central strategies. With regard to the latter, only a limited number of effective rehabilitation techniques to reduce spasticity per se are available at present. Recent evidence suggests that motor recovery after stroke comprises a hierarchical, dynamic framework of interacting mechanisms [3, 4]. Usually after the loss of interhemispheric inhibition from the ipsilesional motor cortex to the contralesional hemisphere following stroke, there is a tendency for overactivity to begin in the contralesional hemisphere soon after the stroke [5, 6]. In the chronic stage, the resulting transcallosal imbalance might hinder cortical reorganization within the ipsilesional hemisphere. This is considered to be a predictor for poor recovery from brain insult [4]. Although its efficacy is still under consideration, repetitive transcranial magnetic stimulation (rTMS) has been used to modulate cortical excitability and harness neuroplasticity in stroke patients to promote motor recovery [7– 12]. High-frequency rTMS facilitates cortical excitability [7, 8], whereas low-frequency rTMS decreases cortical excitability of the stimulated hemisphere [9, 10] and increases cortical excitability of the nonstimulated hemisphere [11, 12]. Thus, the loss of normal interhemispheric inhibition of movement-related brain activation impairs performance by reducing the selectivity of motor unit activation in stroke patients [13]. Therefore, low-frequency rTMS suppresses cortical hyperexcitability in the unaffected hemisphere while high-frequency rTMS activates depressed cortical areas in the 124
Cerebrovasc Dis 2014;37:123–127 DOI: 10.1159/000357421
affected hemisphere, rebalances the interhemispheric inhibition, and corrects impaired performance. In this regard, evidence suggests that hand motor tasks can activate the ipsilateral motor cortex [14]. Moreover, Woldag et al. [15] showed that voluntary activation of the unaffected hand excited the affected hemisphere in stroke patients. The hypothesis tested in this multicenter pilot study was that unaffected arm exercise can activate or inhibit the effects of contralesional motor cortical area and change the function and spasticity of the affected upper limb in stroke patients. To test the hypothesis, we assessed the effects of unaffected arm exercise on upper limb spasticity and function in stroke patients. Materials and Methods Participants A total of 41 consecutive patients with stroke participated in the study. All patients presented with upper limb hemiparesis. Before the onset of stroke, none of the subjects had any medical motorrelated problems due to bone and joint disorders or neurological problems. All subjects had retired from their jobs after the stroke. The inclusion criteria were as follows: (1) history of cerebrovascular accident of at least 6 months, (2) stroke-related paralysis of the upper extremity associated with neuromuscular dysfunction and (3) signing an informed consent based on the institutional ethics review board procedures. Subjects were excluded for the following reasons: (1) if they were medically unstable (e.g. unstable cardiovascular status) and (2) if they suffered significant musculoskeletal problems apart from those related to stroke. For those who were previously admitted to local hospitals, the medical records were obtained to confirm the diagnosis of stroke based on imaging findings (e.g. CT scan and MRI). In addition, the primary care physician was also required to complete a form to confirm the diagnosis of stroke and provide relevant medical history of the subjects (e.g. characteristics of stroke, contraindications to exercise, comorbid conditions). The study procedures were approved by the ethics committee of Wakayama Medical University and adhered to the Declaration of Helsinki. All participants gave written consent before participating in the study. Evaluation of Clinical Status The Functional Independence Measurement [16] was used to describe the functional status on 18 standardized items. The clinical status of each patient was also assessed using the modified Rankin Scale [17] and the National Institutes of Health Stroke Scale [18]. Control and Exercise Intervention Protocol Before the scheduled start of the study, each subject underwent measurement of the maximum work load on an arm crank ergometer (881E Hand Ergometer; Monark, Sweden) using the arm unaffected by stroke while in standing position. The test end point was inability to maintain a cycling cadence of at least 40 rpm [19]. Following an initial rest period of approximately 10 min (baseline),
Sakamoto et al.
Downloaded by: Selçuk Universitesi 193.255.248.150 - 1/29/2015 4:03:52 AM
Introduction
the subject stood for 10 min (control intervention). For exercise, following adequate rest, the subject began cycling an arm crank ergometer at 50% of maximum workload for 10 min using the unaffected arm in standing position. The workload was kept constant in all subjects. The subject maintained a target cadence of 60 rpm throughout the exercise. Baseline and Postintervention Evaluation All subjects underwent blinded evaluation using the modified Ashworth Scale and upper extremity Fugl-Meyer Assessment by a physical therapist who provided the patient with no training to ensure bias-free outcome evaluation. At baseline and after each intervention, the affected arm was physically examined with the modified Ashworth Scale and Fugl-Meyer Assessment. The modified Ashworth Scale grades muscle tone from 0 to 5, with 0 for no increase in muscle tone to 5 for a rigid joint [20]. We used the modified Ashworth Scale to assess spasticity of shoulder adductors, elbow flexors, wrist flexors and finger flexors in the paretic upper extremity. We also used the Fugl-Meyer Assessment to evaluate the severity of motor impairment in the paretic upper extremity [21]. This examination is based on the performance of 33 tasks, which assess the quality of movements, reflex activity and coordination. A score based on a 3-point ordinal scale (0–2) was given to each task, with a higher score indicating less impairment (maximum score, 66). The Fugl-Meyer Assessment is reported to have high interrater reliability (r = 0.99) [22]. Statistical Analysis Data were expressed as mean ± SEM. To facilitate data analysis, the modified Ashworth Scale scores 0, 1, 1+, 2, 3, and 4 were assigned numerical values designated as 0, 1, 2, 3, 4, and 5, respectively. Differences between data recorded at baseline and each intervention were analyzed by ANOVA followed by Scheffe’s F test. A p value
