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The spasticity in the motor and functional disability in adults with post-stroke hemiparetic

A espasticidade no comprometimento motor e funcional de hemiparéticos pós acidente vascular cerebral

Abstract

Introduction:

Spasticity acts as a limiting factor in motor and functional recovery after Stroke, impairing the performance of daily living activities.

Objective:

To analyze the influence of spasticity on main muscle groups and to associate it with motor impairment and functional level of chronic hemiparetic patients after stroke.

Methods:

Twenty-seven chronic hemiparetic patients of both sexes were selected at the Physical Therapy and Occupational Therapy Service of the Unicamp Clinics Hospital. Assessments were carried out in two sessions, in the first one the motor impairment (Fugl-Meyer Assessment - FM) and functional impairment (Barthel Index - BI) were evaluated, and in the second, the degree of spasticity of the main muscle groups (Modified Ashworth Scale - MAS).

Results:

A negative correlation was detected between upper limb spasticity and motor and functional impairment. No muscle group evaluated in the lower limbs showed correlation between muscle tone and the level of impairment of the lower extremity on FM and the functional level measured by BI.

Conclusion:

Spasticity has been shown to be a negative influence factor in the level of motor and functional impairment of the upper limbs of chronic hemiparetic patients after stroke.

Keywords:
Stroke; Hemiparesis; Spasticity

Resumo

Introdução:

A espasticidade atua como um fator limitante na recuperação motora e funcional após o Acidente Vascular Cerebral (AVC), prejudicando a realização das atividades de vida diária.

Objetivo:

Analisar a influência da espasticidade nos principais grupos musculares e associá-la ao comprometimento motor e ao nível funcional de pacientes hemiparéticos crônicos pós-AVC.

Métodos:

Vinte e sete pacientes hemiparéticos crônicos, de ambos os sexos, foram selecionados no Serviço de Fisioterapia e Terapia Ocupacional do Hospital de Clínicas da Unicamp. As avaliações foram realizadas em duas sessões: na primeira foi avaliado o comprometimento motor (Protocolo de Desempenho Físico de Fugl-Meyer - FM) e funcional (Índice de Barthel - IB), e na segunda, o grau de espasticidade dos principais grupos musculares (Escala Modificada de Ashworth - EMA).

Resultados:

Foi detectada uma correlação negativa entre a espasticidade dos membros superiores com o comprometimento motor e funcional. Nenhum grupo muscular avaliado nos membros inferiores apresentou correlação entre o tônus muscular e o nível de comprometimento da subseção da extremidade inferior FM e o nível funcional mensurado pelo IB.

Conclusão:

A espasticidade mostrou ser um fator de influência negativa no nível de comprometimento motor e funcional dos membros superiores de pacientes hemiparéticos crônicos pós-AVC.

Palavras-chave:
Acidente Vascular Cerebral; Hemiparesia; Espasticidade

Introduction

Stroke hemiparetic patients often develop motor disorders associated with imbalance of neural activity, such as spasticity, recognized as a component of upper motor neuron syndrome 11. Ward AB. A Literature review of the pathophysiology and onset of post-stroke spasticity. Eur J Neurol. 2012;19(1):21-7.. Spasticity is defined as increased resistance to passive muscle stretching being dependent on the velocity 22. Urban PP, Wolf T, Uebele M, Marx JJ, Vogt T, Stoeter P, et al. Occurrence and Clinical Predictors of Spasticity After Ischemic Stroke. Stroke. 2010;41(9):2016-20.. Spasticity prevalence after stroke varies from 18% 33. Lundström E, Tere A, Borg J. Prevalence of disabling spasticity one year after first-ever stroke. Eur J Neurol. 2008;15(6):533-9. to 60% 44. Wallesch CW, Maes E, Leconte P, Bartels C. Feasibility study on pharmacoeconomics of botulinum toxin A (Botox) in spasticity following stroke. 3rd European Botulinum Toxin Symposium Abstracts. 1997;1:4., and it is more frequent in the upper limbs than in lower limbs 33. Lundström E, Tere A, Borg J. Prevalence of disabling spasticity one year after first-ever stroke. Eur J Neurol. 2008;15(6):533-9..

Clinically, spasticity is related to increased muscle tone, exaggerated reflexes, pain, and possible joint contractures. Along with these, impairment in motor control, muscle strength deficit and balance deficit lead to several disabilities, influencing the rehabilitation process and performance of functional tasks, as well as the quality of life of individuals with spasticity 55. Williams SA, Reid S, Elliott C, Shipman P, Valentine J. Muscle volume alterations in spastic muscles immediately following botulinum toxin type-A treatment in children with cerebral palsy. Dev Med Child Neurol. 2013;55(9):813-20.), (66. Gracies JM, Brashear A, Jech R, McAllister P, Banach M, Valkovic P, et al. Safety and efficacy of abobotulinumtoxinA for hemiparesis in adults with upper limb spasticity after stroke or traumatic brain injury: a double-blind randomised controlled trial. Lancet Neurol. 2015;14(10):992-1001..

The first clinical instrument developed to measure muscle tone was the Ashworth Scale and the Modified Ashworth Scale 77. Bohannon RW, Smith MB. Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys Ther. 1987;67(2):206-7.), (88. Pandyan AD, Price CIM, Barnes MP, Rodgers H. A review of the properties and limitations of the Ashworth and modified Ashworth scales as measures of spasticity. Clin Rehabil. 1999;13(5):373-83.. They are the most commonly used instruments for this purpose. Despite the shortcomings in manual methods (speed, angle, and acceleration are not standardized), it is the simplest and the most widespread, besides being a validated quantitative instrument that is easy to apply 99. Wood DE, Burridge JH, van Wijck FM, McFadden C, Hitchcock RA, Pandyan AD, et al. Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: a systematic review of the literature. Disabil Rehabil. 2005;27(1-2):19-32..

Some authors 1010. Foley N, Pereira S, Salter K, Fernandez MM, Speechley M, Sequeira K, et al. Treatment With Botulinum Toxin Improves Upper-Extremity Function Post Stroke: A Systematic Review and Meta-Analysis. Arch Phys Med Rehabil. 2013;94(5):977-89.), (1111. Brunnström S. Movement Therapy in Hemiplegia: A Neuropsychological Approach. New York, NY: Harper and Row; 1970. have reported that abnormal reflexes associated with spasticity are the main determinants of motor impairment. It is currently believed that spasticity itself is one of the contributing factors for motor and functional loss after stroke 1212. Sommerfeld DK, Eek EUB, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke . 2004;35(1):134-9., but it is not an isolated agent, since other primary conditions may be associated, such as muscle weakness 1313. Ada L, O’Dwyer N, O’Neill E. Relation between spasticity, weakness and contracture of the elbow flexors and upper limb activity after stroke: An observational study. Disabil Rehabil. 2006;28(13-14):891-7.. Conditions secondary to upper motor neuron injury, such as pain and muscle contracture, also impair the appearance and maintenance of voluntary movements 66. Gracies JM, Brashear A, Jech R, McAllister P, Banach M, Valkovic P, et al. Safety and efficacy of abobotulinumtoxinA for hemiparesis in adults with upper limb spasticity after stroke or traumatic brain injury: a double-blind randomised controlled trial. Lancet Neurol. 2015;14(10):992-1001. and they are, to a certain degree, associated with the acute and/or chronic rehabilitation process that the individuals underwent. In the United States and Europe, these patients receive more support during recovery, especially in the first six or twelve months following stroke 1414. Cramer SC, Koroshetz WJ, Finklestein SP. The case for modality-specific outcome measures in clinical trials of stroke recovery-promoting agents. Stroke . 2007;38(4):1393-5., which is not the case in Brazil.

Thus, the purpose of this study was to analyze the effects of spasticity in the main muscle groups of the upper and lower limbs and to associate it with motor impairment and the functional level of chronic hemiparetic patients after stroke.

Methods

This study was cross-sectional with twenty-seven post-stroke hemiparetic patients recruited at the Physical Therapy and Occupational Therapy Service of the Unicamp Clinics Hospital. They were informed and consented to participate in the research, which was approved by the research ethics committee of Unicamp (#110/2004).

The patients selected had a single unilateral stroke sequela, from non-traumatic origin, for a period of more than six months, of both sexes and aged between 35 and 70 years. Participants had to be able to understand simple instructions and not to have associated orthopedic or neurological conditions. The exclusion criterion was the loss of joint range of motion due to pain or muscle shortening.

Motor impairment was assessed using the Fugl-Meyer Assessmentscale (FM) 1515. Fugl-Meyer AR, Jaasko L, Leyman L, Olsson S, Steglind, S. The post-stroke hemiplegic patient. 1.a method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13-31.. This scale has a total score of 66 points for the upper limb and 34 for the lower limb. The items are scored on ordinal scale: 0 = no achievement, 1 = partial achievement and 2 = complete achievement. FM is a standard instrument, validated in Brazil and widely used in several research centers 1616. Maki T, Quagliato EMAB, Cacho EWA, Paz PSP, Nilce HN, Inoue MME, et al. Estudo de confiabilidade da aplicação da escala de Fugl-Meyer no Brasil. Rev Bras Fisioter. 2006;10(2):179-85.), (1717. Cacho EWA, Melo FRLV, Oliveira R. Avaliação da recuperação motora de pacientes hemiplégicos através do Protocolo de Desempenho Físico de Fugl-Meyer. Rev Neurociênc. 2004;12(2):94-102..

The degree of spasticity was assessed using the Modified Ashworth Scale (MAS) 77. Bohannon RW, Smith MB. Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys Ther. 1987;67(2):206-7. which included the following scores: 0 (zero), no increase in muscle tone; 1 (one) slight increase in tone, manifested by minimal resistance at the end of the range of motion when the affected part is moved in extension or flexion; +1 (+ one), slight increase in muscle tone manifested by blockade, followed by minimal resistance throughout the remainder of the range of motion (less than half); 2 (two), marked increase in muscle tone, despite the absence of joint range of motion impairment, but the affected parts move slowly; 3 (three), considerable increase of muscle tone hindering passive movement; 4 (four), stiffness in the affected parts for flexion or extension. The muscle groups evaluated in the upper limb were: flexors, extensors, adductors, abductors, internal and external rotators of the shoulder, elbow flexors and extensors, forearm pronators and supinators, and flexors and extensors of wrist and fingers. In the lower limb: flexors, extensors, adductors, abductors, internal and external rotators of the hip, knee flexors and extensors, plantar flexors and dorsiflexors. The presence of spasticity was defined as a score ≥ 1 in a muscle group.

Barthel Index (BI) evaluates activities of daily living (ADLs), reaching a total of 100 points for individuals who are independent to perform the tasks 1818. Mahoney FI, Barthel D. Functional evaluation: the Barthel Index. Md State Med J. 1965;14:56-61.. The BI is a frequently used measure with well-established validity, reliability and acceptability 1919. Duffy L, Gajree S, Langhorne P, Stott DJ, Quinn TJ. Reliability (Inter-rater Agreement) of the Barthel Index for Assessment of Stroke Survivors. Stroke . 2013;44:462-8..

Evaluations were carried out in two sessions (on different days). In the first one, FM and BIwere applied, and on the following day the muscular tone evaluation was performed in dorsal decubitus, by passive movement of the upper limb (shoulder, elbow, forearm, wrist and fingers) and lower limb (hip, knee and ankle), according to MAS criteria. The evaluations were performed by two experienced physical therapists familiar with the scales.

Descriptive statistics of continuous variables were established by mean values and standard deviation. Correlation between scores was then performed using Spearman Correlation Coefficient. This coefficient was used due to the absence of normal distribution and reduced sample size. The significance level adopted for the statistical tests was 5% (p < 0.05).

Results

Among the selected patients, 40.7% (N = 11) were female and 59.3% (N = 16) males, mean age of 49.48 (± 11.49) years, and mean time of 3.43 (± 3.18) years post-stroke. Left ischemic stroke had higher prevalence (40.7%/N = 11). FM mean score in the upper limb was 33.81 (± 19.68), in the lower limb was 18.55 (± 8.34), presenting a total score of 52.37 (± 24.72). In BI, the mean was 91.11 (± 6.41).

Spasticity in the upper limb was detected in 66.6% (N = 18) of the 27 patients evaluated. Muscle groups of forearm pronators and flexors of the elbow, wrist and fingers were spastic in more than 60% of the patients (N = 17) (Table 1). At the lower extremity, spasticity in plantar flexors occurred in 66.6% of the patients.

Table 1
Frequency and percentage of spasticity in upper and lower limb muscle groups

Six subjects did not present spasticity in any muscle groups of the evaluated upper limb (FM - upper limb subsection 61.5 ± 2.96 / BI 98.33 ± 2.58). Seven subjects scored 0 at Ashworth for all lower limb muscle groups (FM - lower limb subsection 22.12 ± 11.21 / BI 93.75 ± 6.49).

Negative correlation was found between muscle tone of the extensors, adductors and internal rotators of the shoulder, flexors and extensors of the elbow, and flexors of the wrist and fingers, and the level of motor impairment in the upper limb on FM. Regarding functional level, negative correlation was also observed between the muscle tone of extensors, adductors and internal rotators of the shoulder and flexors and extensors of the elbow (Table 2).

Table 2
Statistical significance between the Modified Ashworth Scale - MAS scores with the Fugl-Meyer Assessment - FM and the Barthel Index - BI

No muscle group assessed in the lower limbs showed correlation between muscle tone and level of impairment of lower extremity on FM and the functional level measured by BI.

Significant positive correlation was found between total FM and BI (r = 0.6169; p = 0.0001), and between the upper limb FM subsection and BI (r = 0.6747; p = 0.0001).

Discussion

Spasticity is one of the main factors contributing to the loss of selective motor control, especially in individuals who manifest severe motor impairment after stroke 1212. Sommerfeld DK, Eek EUB, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke . 2004;35(1):134-9.. According to FM scale,upper limbs total motor score of patients in this study shows a level of impairment classified as severe to moderate (score between 5 and 46) 2020. Cirstea MC, Ptito A, Levin MF. Arm reaching improvements with short-term practice depend on the severity of the motor deficit in stroke. Exp Brain Res. 2003;152(4):476-88.. The lower limb presented FM mean score corresponding to 54.56% of motor recovery. Movement disorders following stroke may also be due to loss of strength and motor ability, because of disconnected interarticular coordination or pathological synergies 2121. Jarrassé N, Proietti T, Crocher V, Robertson J, Sahbani A, Morel G, et al. Robotic exoskeletons: a perspective for the rehabilitation of arm coordination in stroke patients. Front Hum Neurosci. 2014;8:947..

In a study on the prevalence of spasticity, 20% of 66 patients evaluated had some level of spasticity. This number increased to 34% when considering hemiparetic subjects 2222. Welmer Ak, von Arbin M, Holmquist LW, Sommerfeld DK. Spasticity and it association with functioning and heath-related quality of life 18 months after stroke. Cerebrovasc Dis. 2006;21(4):247-53.. Lundströnet al. 33. Lundström E, Tere A, Borg J. Prevalence of disabling spasticity one year after first-ever stroke. Eur J Neurol. 2008;15(6):533-9. observed that 17% of the patients had upper limb spasticity after one year of stroke. In this study, 66.6% of the patients presented upper and/or lower limb spasticity. These values are above the average of other studies and may be explained by the high level of motor impairment (measured by total FM = 52.37 ± 24.52) of the selected patients and by the effects of lesion chronicity. According to Thilmannet al. 2323. Thilmann AF, Fellows SJ, Garms E. The mechanism of spastic muscle hypertonus: variation in reflex gain over the time course of spasticity. Brain. 1991;114(Pt 1A):233-44., after three months of stroke, spasticity seems to be also due to intrinsic factors, such as decrease in the number of sarcomeres in series that result in slow movement and difficulty in selectivity (co-contraction) 2424. Lieber RL, Frieden J. Spasticity causes a fundamental rearrangement of muscle-joint interaction. Muscle Nerve. 2002;25(2):265-70.. In this study, all patients were chronic, that is, with more than six months of injury. Therefore, we can infer that the difficulty in performing voluntary movements (which caused a reduced score in FM scale) may be due to these neuromuscular changes occurring in the chronic phase after stroke, and also to the control deficit in superior motoneurons firing.

Differently from other studies, the sample studied here showed similar spasticity in both extremities, but it was present in more muscles of the upper extremity than in the lower one. It is not yet defined why spasticity affects upper limb motor performance more than lower limbs 2525. Lin FM, Sabbahi M. Correlation of spasticity with hyperactive stretch reflexes and motor dysfunction in hemiplegia. Arch Phys Med Rehabil. 1999;80(5):526-30.. It is believed that it may be due to the fact that locomotion is also present in spinal levels and that spasticity may help orthostatism, contributing to maintain body weight 99. Wood DE, Burridge JH, van Wijck FM, McFadden C, Hitchcock RA, Pandyan AD, et al. Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: a systematic review of the literature. Disabil Rehabil. 2005;27(1-2):19-32.), (2525. Lin FM, Sabbahi M. Correlation of spasticity with hyperactive stretch reflexes and motor dysfunction in hemiplegia. Arch Phys Med Rehabil. 1999;80(5):526-30..

When we selected only patients who did not present spasticity in any of the muscle groups of the evaluated upper limb (six subjects), we noticed that FM scores in the subsection of upper limb and BI (FM 61.5 ± 2.96 / BI 98.33 ± 2.58) were higher than the rest of the group (FM 25.90 ± 14.34 / BI 89.4 ± 5.61). Lundströnet al. 33. Lundström E, Tere A, Borg J. Prevalence of disabling spasticity one year after first-ever stroke. Eur J Neurol. 2008;15(6):533-9. and Watkins et al. 2626. Watkins CL, Leathley MJ, Gregson JM, Smith TL, Sharma AK. Prevalence of spasticity post stroke. Clin Rehabil. 2002;16(5):515-22. identified that the rate of patients dependent on activities of daily living according to BI was higher in those patients with spasticity when compared to those without spasticity. In contrast, Sommerfeld et al. 1212. Sommerfeld DK, Eek EUB, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke . 2004;35(1):134-9. demonstrated that severe motor and functional problems are observed with the same frequency in spastic and non-spastic patients. The exact influence of spasticity on motor impairment and limitations after stroke is difficult to measure because the level of spasticity may change according to the positioning and the task demands 1212. Sommerfeld DK, Eek EUB, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke . 2004;35(1):134-9..

The medial descending pathways (medial corticospinal, medial and lateral vestibulospinal,tectospinal and medialreticulospinal) and lateral descending pathways (lateral corticospinal, rubrospinal and lateral reticulospinal) commands the axial and distal muscles. After stroke, some of these pathways may be damaged, leading to loss of dexterity, strength and voluntary movement. Several plastic processes of the central nervous system act after injury in order to restore motor and functional control, such as reorganization of intracortical connections, appearance of collateral cortico-spinal projections from other regions of the primary motor cortex or other areas of the brain,increased cortical activation of descending pathways from the midbrain and increased activity of ipsilateral cortico-spinal projections from the unaffected cortex 2727. Bradnam LV, Stinear CM, Byblow WD. Ipsilateral motor pathways after stroke: implications for non-invasive brain stimulation. Front Hum Neurosci. 2013;7:184.), (2828. Turton A. Mechanisms for recovery of hand and arm function after stroke: a review of evidence from studies using non-invasive investigative techniques. Br J Occup Ther. 1998;61(8):359-64.. However, the loss of distal selective motricity due to injury to the cortico-spinal tract is not repaired and/or replaced 2929. Katz RT, Rovai GP, Brait C, Rymer WZ. Objective quantification of spasticity hypertonia: correlation with clinical findings. Arch Phys Med Rehabil. 1992;73(4):339-47.. It explains why spasticity, which is one of the main effects of upper motor neuron injury, was found mainly in distal muscles of the upper and lower limbs in this study (Table 1). Also on the descending pathways, midbrain motor areas lose influence of cortical projections after stroke, leading to abnormal control over the muscles and causing the classic and antigravity pattern of extensor muscles of the lower limbs and flexors of the upper limbs 2828. Turton A. Mechanisms for recovery of hand and arm function after stroke: a review of evidence from studies using non-invasive investigative techniques. Br J Occup Ther. 1998;61(8):359-64.. This antigravity pattern is present in patients from this study, and may be observed by the higher spasticity incidence in muscles that compose this abnormal synergy.

The level of upper limb motor impairment and the functional capacity of hemiparetic patients in this study were affected by the presence of spasticity. Those with spasticity showed decreased FM and BI scores. Lin et al. 2525. Lin FM, Sabbahi M. Correlation of spasticity with hyperactive stretch reflexes and motor dysfunction in hemiplegia. Arch Phys Med Rehabil. 1999;80(5):526-30., using different measurement instruments from the ones in this study, reported significant inverse correlation between the degree of spasticity of the wrist joint and voluntary motor performance, including functional tasks such as Box and Blocks test. Watkins et al. 2626. Watkins CL, Leathley MJ, Gregson JM, Smith TL, Sharma AK. Prevalence of spasticity post stroke. Clin Rehabil. 2002;16(5):515-22. also reported that patients with spasticity (measured by MAS) were more functionally impaired than those without spasticity. Welmer et al. 2222. Welmer Ak, von Arbin M, Holmquist LW, Sommerfeld DK. Spasticity and it association with functioning and heath-related quality of life 18 months after stroke. Cerebrovasc Dis. 2006;21(4):247-53. correlated upper limb spasticity (measured by MAS) with measures of voluntary motor mobility (Birgitta Lindmark Motor Assessment Scale - LMAS, Rivermead Mobility Index - RMI) and BI, and found moderate to high correlation.

Regarding lower limbs, there was no relationship between spasticity and the level of motor and functional impairment of hemiparetic individuals. This finding is similar to those of Welmer et al. 2222. Welmer Ak, von Arbin M, Holmquist LW, Sommerfeld DK. Spasticity and it association with functioning and heath-related quality of life 18 months after stroke. Cerebrovasc Dis. 2006;21(4):247-53. that reported low correlation between lower limbs spasticity with RMI and BI. Katz et al. 2929. Katz RT, Rovai GP, Brait C, Rymer WZ. Objective quantification of spasticity hypertonia: correlation with clinical findings. Arch Phys Med Rehabil. 1992;73(4):339-47. also observed no correlation between the degree of spasticity of the lower extremity muscles and the scores on FM scale.

Correlations between spasticity and motor and functional impairment in the upper and lower limbs are not similar due to some factors. First, spasticity may manifest differently in different muscle groups, since skill, motor dexterity, and functional requirements are different for each structure. Second, measurement tools fail because they are not able to differentiate between a functional motor response and a compensatory strategy 3030. Oliveira R, Cacho EWA, Borges G. Post-stroke motor and functional evaluations: a clinical correlation using Fugl-Meyer Assessment Scale, Berg Balance Scale and Barthel Index. Arq Neuropsiquiatr. 2006;64(3B):731-5.. In addition, it is important to highlight that several factors may contribute to this event, such as injury time, level of motor impairment, intrinsic (non-neural) muscular factors, among others 1313. Ada L, O’Dwyer N, O’Neill E. Relation between spasticity, weakness and contracture of the elbow flexors and upper limb activity after stroke: An observational study. Disabil Rehabil. 2006;28(13-14):891-7..

Similar to that found by Oliveira et al. 3030. Oliveira R, Cacho EWA, Borges G. Post-stroke motor and functional evaluations: a clinical correlation using Fugl-Meyer Assessment Scale, Berg Balance Scale and Barthel Index. Arq Neuropsiquiatr. 2006;64(3B):731-5., it was observed that a better FM score is also accompanied by an increase in BI, indicating that motor impairment is inversely proportional to satisfactory functional performance.

Conclusion

Thus, spasticity is characterized as a factor of negative influence on motor and functional impairment of the upper limbs of chronic hemiparetic patients after stroke, that is, spasticity acts as a limiting factor for motor and functional recovery.

Acknowledgments

We thank São Paulo Research Foundation (FAPESP) (#06/61199-5) and the National Council for Scientific and Technological Development (CNPq) (#302189/2004-1) for financial support.

References

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    Ward AB. A Literature review of the pathophysiology and onset of post-stroke spasticity. Eur J Neurol. 2012;19(1):21-7.
  • 2
    Urban PP, Wolf T, Uebele M, Marx JJ, Vogt T, Stoeter P, et al. Occurrence and Clinical Predictors of Spasticity After Ischemic Stroke. Stroke. 2010;41(9):2016-20.
  • 3
    Lundström E, Tere A, Borg J. Prevalence of disabling spasticity one year after first-ever stroke. Eur J Neurol. 2008;15(6):533-9.
  • 4
    Wallesch CW, Maes E, Leconte P, Bartels C. Feasibility study on pharmacoeconomics of botulinum toxin A (Botox) in spasticity following stroke. 3rd European Botulinum Toxin Symposium Abstracts. 1997;1:4.
  • 5
    Williams SA, Reid S, Elliott C, Shipman P, Valentine J. Muscle volume alterations in spastic muscles immediately following botulinum toxin type-A treatment in children with cerebral palsy. Dev Med Child Neurol. 2013;55(9):813-20.
  • 6
    Gracies JM, Brashear A, Jech R, McAllister P, Banach M, Valkovic P, et al. Safety and efficacy of abobotulinumtoxinA for hemiparesis in adults with upper limb spasticity after stroke or traumatic brain injury: a double-blind randomised controlled trial. Lancet Neurol. 2015;14(10):992-1001.
  • 7
    Bohannon RW, Smith MB. Interrater reliability of a Modified Ashworth Scale of muscle spasticity. Phys Ther. 1987;67(2):206-7.
  • 8
    Pandyan AD, Price CIM, Barnes MP, Rodgers H. A review of the properties and limitations of the Ashworth and modified Ashworth scales as measures of spasticity. Clin Rehabil. 1999;13(5):373-83.
  • 9
    Wood DE, Burridge JH, van Wijck FM, McFadden C, Hitchcock RA, Pandyan AD, et al. Biomechanical approaches applied to the lower and upper limb for the measurement of spasticity: a systematic review of the literature. Disabil Rehabil. 2005;27(1-2):19-32.
  • 10
    Foley N, Pereira S, Salter K, Fernandez MM, Speechley M, Sequeira K, et al. Treatment With Botulinum Toxin Improves Upper-Extremity Function Post Stroke: A Systematic Review and Meta-Analysis. Arch Phys Med Rehabil. 2013;94(5):977-89.
  • 11
    Brunnström S. Movement Therapy in Hemiplegia: A Neuropsychological Approach. New York, NY: Harper and Row; 1970.
  • 12
    Sommerfeld DK, Eek EUB, Svensson AK, Holmqvist LW, von Arbin MH. Spasticity after stroke: its occurrence and association with motor impairments and activity limitations. Stroke . 2004;35(1):134-9.
  • 13
    Ada L, O’Dwyer N, O’Neill E. Relation between spasticity, weakness and contracture of the elbow flexors and upper limb activity after stroke: An observational study. Disabil Rehabil. 2006;28(13-14):891-7.
  • 14
    Cramer SC, Koroshetz WJ, Finklestein SP. The case for modality-specific outcome measures in clinical trials of stroke recovery-promoting agents. Stroke . 2007;38(4):1393-5.
  • 15
    Fugl-Meyer AR, Jaasko L, Leyman L, Olsson S, Steglind, S. The post-stroke hemiplegic patient. 1.a method for evaluation of physical performance. Scand J Rehabil Med. 1975;7(1):13-31.
  • 16
    Maki T, Quagliato EMAB, Cacho EWA, Paz PSP, Nilce HN, Inoue MME, et al. Estudo de confiabilidade da aplicação da escala de Fugl-Meyer no Brasil. Rev Bras Fisioter. 2006;10(2):179-85.
  • 17
    Cacho EWA, Melo FRLV, Oliveira R. Avaliação da recuperação motora de pacientes hemiplégicos através do Protocolo de Desempenho Físico de Fugl-Meyer. Rev Neurociênc. 2004;12(2):94-102.
  • 18
    Mahoney FI, Barthel D. Functional evaluation: the Barthel Index. Md State Med J. 1965;14:56-61.
  • 19
    Duffy L, Gajree S, Langhorne P, Stott DJ, Quinn TJ. Reliability (Inter-rater Agreement) of the Barthel Index for Assessment of Stroke Survivors. Stroke . 2013;44:462-8.
  • 20
    Cirstea MC, Ptito A, Levin MF. Arm reaching improvements with short-term practice depend on the severity of the motor deficit in stroke. Exp Brain Res. 2003;152(4):476-88.
  • 21
    Jarrassé N, Proietti T, Crocher V, Robertson J, Sahbani A, Morel G, et al. Robotic exoskeletons: a perspective for the rehabilitation of arm coordination in stroke patients. Front Hum Neurosci. 2014;8:947.
  • 22
    Welmer Ak, von Arbin M, Holmquist LW, Sommerfeld DK. Spasticity and it association with functioning and heath-related quality of life 18 months after stroke. Cerebrovasc Dis. 2006;21(4):247-53.
  • 23
    Thilmann AF, Fellows SJ, Garms E. The mechanism of spastic muscle hypertonus: variation in reflex gain over the time course of spasticity. Brain. 1991;114(Pt 1A):233-44.
  • 24
    Lieber RL, Frieden J. Spasticity causes a fundamental rearrangement of muscle-joint interaction. Muscle Nerve. 2002;25(2):265-70.
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Publication Dates

  • Publication in this collection
    Oct-Dec 2017

History

  • Received
    16 Dec 2015
  • Accepted
    16 Mar 2017
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