Reduction of spastic hypertonia during repeated passive knee movements in stroke patients
Accepted: August 28, 2001;
Abstract
Nuyens GE, De Weerdt WJ, Spaepen AJ Jr, Kiekens C, Feys HM. Reduction of spastic hypertonia during repeated passive knee movements in stroke patients. Arch Phys Med Rehabil 2002;83:930-5. Objectives: To quantify changes in spastic hypertonia during repeated passive isokinetic knee movements in stroke patients and to assess the role of muscle activity. Design: A between-groups design with repeated measures. Setting: Rehabilitation center for stroke patients. Participants: Ten stroke patients with hypertonia and 10 healthy subjects matched for age and gender.Intervention: With an isokinetic apparatus, movements were imposed on the knee in series of 10 repetitions at speeds of 60°/s, 180°/s, and 300°/s. Main Outcome Measures: Spastic hypertonia was assessed on the basis of torque measurement and electromyographic activity of the quadriceps, hamstrings, and gastrocnemius muscles. Results:Compared with the controls, stroke patients presented a significantly stronger torque reduction during the mid- and endphases of movements at all speeds tested (P<.05). The strongest torque decline occurred during knee flexion and during the first movements. The effect increased toward the end phase of movements and with increasing speeds. The effect of movement repetitions on torque measurements was unchanged after electromyographic activity was included in the statistical analysis, except during extension movements at 180°/s and 300°/s. Conclusion: Passive movements of the knee induced a decrease of spastic hypertonia in stroke patients through a combination of reflexive and mechanical factors. The role of these mechanisms is velocity dependent and differs for flexion and extension movements. © 2002 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation
REHABILITATION AFTER STROKE remains a challenge. Exercise therapy is commonly used to help the stroke survivor recover from physiologic impairments caused by the lesion of the central nervous system. Randomized controlled studies1, 2 have shown that intensive treatment may help improve spontaneous recovery of motor function. When spastic hypertonia is identified, joint mobilizations and muscle stretching are considered an integral part of the patient's daily management. Clinical evidence has shown that regular mobilizations help prevent contractures and can reduce the severity of spastic tone for several hours.3 Most concepts specifically developed for the rehabilitation of stroke patients, such as neurodevelopmental therapy, include passive movement of limbs as a substantial technique to reduce muscle hypertonia.4 Surprisingly, no studies have quantitatively reported the specific effect of repeated movements on hypertonia in stroke patients.
The mechanism for reduction of muscle tone as a response to repeated movements is not clear. Habituation of reflex activity to repeated stretch may result from a decrease in synaptic transmission caused by inactivation of presynaptic calcium channels.3 However, the exclusive role of neurophysiologic mechanisms as a cause of enhanced response to stretch is debated.5 Several researchers have found that increased stretch responses were not necessarily accompanied by enhanced electromyographic activity. Lamontagne et al6 found that a decrease in resistance during repeated passive movements without concurrent changes in electromyographic activity was attributable to thixotropic characteristics of the stretched tissues. The term thixotropy refers to the property of certain systems becoming less viscous when shaken and then returning to the original viscosity after a period of not being disturbed.7 In muscles, thixotropic changes may occur as a consequence of motion by tearing the cross-bridges between the actin and myosin filaments. When the agitation ceases, the bridges are reformed, and the muscle becomes stiffer again. Other researchers8, 9, 10 have concluded that mechanical changes in the musculotendinous unit may also be involved. The finding that hypertonia is not necessarily accompanied by enhanced electromyographic activity has caused some investigators to question the use of treatment modalities focused on the inhibition of reflexive responses in the treatment of spastic hypertonia.8
The debate on the relative role of neurophysiologic and mechanical mechanisms in enhanced response to stretch may be partially attributed to a discrepancy in terminology used.5 Spasticity has been defined as “a motor disorder characterized by a velocity dependent increase in tonic stretch reflexes (muscle tone) with exaggerated tendon jerks, resulting from hyperexcitability of the stretch reflex, as one component of the upper motor neuron syndrome.”11 For clinical assessment, however, spasticity has been operationally defined as increased resistance to passive movement.12 The lack of consensus concerning the pathogenesis and definition of spastic hypertonia shows the complexity of this phenomenon and makes it difficult to quantify. Studies have indicated distinct manifestations of hypertonia in active or passive movements13 and in different movement speeds,14 joints,15 test positions,16 or pathologies.17
Much effort has been put in to the development of strategies to manage spastic hypertonia by means of exercise therapy, medication, and surgery. Basic research on the features of hypertonia and on the mechanism of therapeutic interventions may help to develop a rationale for rehabilitation in a larger context.
Our study sought to assess the effect of movement repetitions on spastic hypertonia in stroke patients on the basis of torque measurements and electromyographic activity. The first hypothesis tested was that resistive torque would occur during the initial movements in stroke patients and be reduced during repeated movements and that there would be no torque reduction in the healthy subjects. Second, we hypothesized that if torque changes did occur in the subjects with spastic hypertonia, they would parallel changes in the electromyographic activity of the stretched muscles.
Methods
Subject inclusion criteria
The stroke patients participating in this study were recruited from the University Hospitals of Leuven in Belgium. Muscle tone of the affected lower limb was assessed clinically in 50 subjects. Persons were eligible for further participation if they had hypertonia during knee flexion and/or extension, and a minimal score of 2 on the Ashworth Scale18 (table 1). Exclusion criteria consisted of (1) having experienced more than 1 stroke, (2) an unstable clinical condition or major comorbidity, (3) pain during clinical assessment, (4) orthopedic problems in the lower limb, and (5) knee range of motion (ROM) less than 90° within the total knee joint ROM. The control group consisted of healthy persons matched for age and gender with the patients. All subjects gave their written consent before they were included in the study. The project was approved by the institutional review committee.
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Experimental protocol and measurement
Biomechanical tests were performed with an isokinetic apparatus that incorporated a computer-controlled, electric servomotora; a strain gauge bridge torquemeterb; and an isolated biomedical electromyography amplifier.c The torquemeter shaft was connected to a rotating lever for the tested limb to be attached. Subjects sat on a bench with the back supported and the thigh fixed on the bench with a Velcro® strap. The ankle was fixed in a 90° position within an orthosis. The knee joint was visually aligned with the rotation axis of the lever, and the lower leg was attached just above the malleoli to the distal end of the lever.
In this position, muscle tone in knee flexors and extensors was first assessed clinically by a physiotherapist. A score was assigned according to the Ashworth Scale (table 1). Then, flexion and extension movements were imposed on the knee by the electromotor at 60°/s, 180°/s, and 300°/s in a series of 10 consecutive repetitions per velocity. Movement speeds were not randomized for safety reasons. The lowest speed, 60°/s, was always applied first. The test sessions were continued with speeds 180° and 300°/s, respectively, only if movements were pain free. The average interval between each flexion and extension movement was 5 seconds. Accelerations and decelerations were set at 3000°/s2. These very high values were chosen to achieve constant movement speeds for a maximal ROM. After the biomechanical tests, the clinical assessment of muscle tone was repeated. Subjects were instructed to relax the leg throughout the test procedure.
During the biomechanical tests, torque and velocity of movement as well as electromyography of the quadriceps femoris, hamstrings, and gastrocnemius medialis muscles were recorded at 1000 samples per second. Electrode placement was standardized.19 The electromyograph was registered with bipolar Ag-AgCl surface electrodes,d preamplified with active electrodese (amplitude=54dB; common mode rejection ratio=100dB), and amplified with a bandpass filter (5–450Hz). The raw electromyographic data were converted to muscle activity with a differentiation technique.20 Data were processed with a Microstar data-acquisition card,f with a resolution of 12-bits and an onboard coprocessor.
Data analysis
The analysis was performed on data registered during the isokinetic phase of the test movements. The term isokineticrefers to the situation when a force is applied at a constant angular velocity against a body segment. Measurements during acceleration and deceleration phases of the movements were omitted because they were proven to be strongly affected by inertial forces.13 The isokinetic phase of the movements was divided into 3 equal parts, which are further referred to as the initial phase, midphase, and endphase of the movements. Hence, 3 average values of torque and electromyographic activity were calculated for each test.
Change of torque over a series of 10 test repetitions was calculated by subtracting the torque measured during the first test movement from the torque registered during the last movement (T1 - T10). Torque changes after the initial test movement were determined in a similar way by calculating T2 - T10, T3 - T10,..., T9 - T10. This subtraction procedure provides a way to correct torque measurements for influences of gravitational forces.
To compare the torque variations during test repetitions between the stroke patients and the healthy subjects, we used a linear mixed model.21 A mixed model provides a suitable approach to complex covariation structures of data, which occur in case of many test repetitions. To investigate whether the changes in torque measurement were paralleled by the activity of the stretched muscle groups, the quadriceps muscle during knee flexion, and the hamstrings and triceps surae during knee extension, we constructed another linear mixed model that included both torque measurements and electromyographic activity.
Differences were considered statistically significant at P≤.05. All analyses were performed with SAS, version 6.12.g
Results
Participants
Of 50 stroke patients, 18 were assigned an Ashworth score of 2 or more during clinical testing of hypertonia in the affected knee. Eight subjects were excluded from further testing because of their clinical condition (n=6) or because they did not want to participate in the biomechanical testing procedure (n=2). In the 10 patients who were eligible for biomechanical testing, the median Ashworth score was 2, ranging between 0 and 3 for the flexors and between 0 and 2 for the extensors of the knee. Seven participants had left-side hemiplegia and 3 had right-side hemiplegia. The type of stroke was ischemic in 9 patients and hemorrhagic in 1. The mean disease duration in the patient group was 19±12 months. The mean Barthel Index, representing overall functional disability, was 80 (range, 30–100/100). The mean age in the patient group was 63±10 years. The 10 healthy subjects in the control group had a mean age of 62±8 years. Each group had 7 men and 3 women.
Torque responses during repeated movements
In stroke patients, resistive torque decreased as movements were repeated in all test conditions, knee flexion, and extension at speeds of 60°, 180°, and 300°/s. Mean differences of torque between the first and the tenth test movements (T1 - T10) varied between .32 and 2.75Nm during knee extension and between .91 and 10.34Nm during knee flexion. The strongest decline in resistive torque occurred during the first few movements of the test repetitions. The torque measurements further revealed that the most pronounced changes occurred during the endphases of the movements and during movements at the highest speeds. In the control subjects, some resistive torque was also found in the initial test repetitions, especially during knee flexion at 180° and 300°/s. Maximal torque differences between the first and tenth test movements were 1.02 and 4.26Nm for knee extension and knee flexion, respectively.
Figure 1 shows torque measurements during the 10 repeated movements in stroke patients and control subjects.
Fig. 1
Torque alterations during repeated knee movements. (A) Knee extension at 60°/s, (B) 180°/s, (C) 300°/s, and (D) knee flexion at 60°/s, (E) 180°/s, and (F) 300°/s in 10 subjects with stroke and 10 healthy subjects.
Table 2 presents the statistical comparison of torque changes during movement repetitions between both groups by the interaction repetitions groups. Compared with the control subjects, patients presented a significantly stronger reduction (P<.05) in the torques during the mid- and endphases of all the test movements. After exclusion of the first 3 movements from the sequence, no significant differences were found between the torque alterations measured during repeated movements in the stroke patients and in the control group.
| Test Movement | Knee Extension Interaction Repetition Group | Knee Flexion Interaction Repetition Group | |||
|---|---|---|---|---|---|
| Velocity (°/s) | Phase | Without EMG (P) | With EMG* (P) | Without EMG (P) | With EMG* (P) |
| 60 | Initial | .30 | .005 | .002 | .0001 |
| 60 | Mid | .007 | .01 | .0001 | .0001 |
| 60 | End | .04 | .002 | .03 | .0001 |
| 180 | Initial | .40 | .18 | .11 | .0001 |
| 180 | Mid | .0001 | .34† | .003 | .0001 |
| 180 | End | .0001 | .24† | .003 | .0001 |
| 300 | Initial | .35 | .006 | .07 | .0001 |
| 300 | Mid | .03 | .10† | .01 | .0001 |
| 300 | End | .0001 | .14† | .0001 | .0001 |
| * Interaction between repetitions and groups controlled for electromyographic activity in the stretched muscle groups: the hamstrings and gastrocnemius medialis muscles during knee extension and the quadriceps during knee flexion. † P value test points where the electromyographic activity of the stretched muscle groups was identified as the explanatory factor for torque variations by the statistical model. | |||||
Note. Results of a linear mixed model.
Abbreviation: EMG, electromyography.
Electromyographic activity of stretched muscles during repeated movements
During the repeated movements, muscle activity paralleled the variations in torque measurements for some test conditions but not for others. Examples of variations in torque and electromyographic activity are shown in figure 2.
Fig. 2
Torque and electromyographic activity of the stretched muscle groups during repeated knee extension at (A) 60°/s and (B) 300°/s in 10 subjects with stroke.
The statistical model showed that, for extension movements at 180° and 300°/s, torque changes between patient and control groups became nonsignificant after electromyographic activity was taken into account (table 2). For the other test conditions, significant differences in torque variations between groups remained significant even after the electromyographic activity of the stretched muscle groups was included in the statistical model.
Discussion
The common use of muscle stretching and joint mobilization as a physiotherapeutic intervention in spastic hypertonia is based on the clinical experience that resistance decreases during repeated passive movements. Our results provide a quantitative and objective endorsement of this clinical finding. Compared with the healthy subjects, the stroke patients presented a significantly more pronounced decreased resistance to passive movements of the knee at the 3 speeds, both during flexion and extension. The differences between the 2 groups occurred mainly during the first test movements. In the context of rehabilitation, this may imply that, if spastic hypertonia in the knee hinders particular functions, such as walking or transfers, a few mobilizations of the knee might be sufficient to decrease the manifestation of the impairment. However, the fact that the difference between the 2 groups faded after 3 test repetitions does not imply that 3 knee movements would be sufficient to prevent stiffening of the joint or to produce a lasting reduction of muscle tone. Further research would be necessary to quantify the long-term effects of mobilizations of the joints in persons with spastic hypertonia.
The concurrent registration of electromyographic activity in the stretched muscle groups during the tests indicated, as expected, that muscle activity had a role in the generation of increased resistance during passive movements. To investigate whether electromyographic activity was the causal factor of differences in torque responses between the patients and the healthy subjects, the P values of the interaction between test repetitions and groups were compared with and without the electromyographic activity as a covariate in the analysis model. It appeared that the differences in torque response found during the mid- and endphases of all test movements remained significant except for extension movements at 180° and 300°/s after the electromyographic activity was taken into account (table 2). These results imply that besides reflex activity, other mechanisms were responsible for the increased resistance to passive stretch during extension at 60°/s and during the flexion movements. It has been proposed that the resistance measured during stretch of a noncontracting muscle originates from viscoelastic components of the musculotendinous unit, including thixotropic features.6, 22, 23 Others8 have suggested that hypertonia could be a result of changes in the mechanical properties of muscles, such as atrophy of phasic motor units and hypertrophy of tonic units.
The finding that the impact of reflexive reactions on torque differs between test conditions adds a new dimension to the debate on the role of neurophysiologic and mechanical mechanisms in the pathogenesis of spastic hypertonia. Our study revealed that different causal mechanisms may be involved when hypertonia is investigated in different test conditions, in this case speed or direction of the movement. The observation that reflexive mechanisms were the explaining factor of hypertonia during extension but not during flexion of the knee presents a striking parallelism with reports of studies involving active movements.24, 25 While investigating reflexes of gastrocnemius and tibialis anterior muscles during stance in 11 subjects with spastic hemiparesis, Berger et al24 found that electromyographic activity was more involved in hypertonia during plantarflexion than during dorsiflexion of the ankle joint. Differences between flexors and extensors were also reported for the upper limb in a study25 of 15 subjects with spastic hemiparesis. Increased resistance to movement without electromyographic activity was more pronounced in the flexors than in the extensor muscles of the elbow during active movements. Dietz et al25 suggested that their findings might be attributed to differences in muscle mass in favor of the antigravity muscles or, alternatively, to a differential control of flexor and extensor muscles by the supraspinal centers. Similar mechanisms could be responsible for the typical Wernicke-Mann posture in subjects with spastic hemiparesis, with a flexed arm and an extended leg on the spastic side.25
The finding that increased resistance to passive movement may be determined by both reflexive responses and mechanical features calls into question the validity of the operational definition of muscle tone commonly used in assessment. Clinical and biomechanical testing of spastic hypertonia is traditionally based on the assumption that muscle tone, inferring reflexive response, can be measured by the resistance to passive joint movement. Either the term muscle tone needs to be interpreted in a larger context, including mechanical responses of both contractile and noncontractile tissues, or electromyographic measurement should be included in the test procedure to differentiate reflexive from mechanical restraints during passive movements.
The biomechanical tests included 3 movement speeds. The order of testing was not randomized for speed. Tests at 60°/s were performed first, then tests at 180°/s, and finally those at 300°/s. This procedure was followed for safety reasons. Patients with hypertonia cannot be subjected to high-movement speeds at the onset of testing. The use of a nonrandomized procedure implies that the torque decrease during tests at high speeds may have been underestimated by mobilizations at lower speeds. Nevertheless, the torque decrease during the repeated movements at 180° and 300°/s was found to be stronger than during the tests at 60°/s (fig 1).
Only 20 subjects were included in this study, which implies that the power of statistical tests may have been limited. Yet, the response to mobilizations was significantly stronger in the stroke patients compared with the control group. Further studies could be useful in identifying factors that may influence the effect of mobilization on hypertonia, such as gender, age, pathogenesis of the stroke, disease duration, or treatment conditions.
Conclusion
Our study supports the common use of mobilization in the management of spastic hypertonia. However, it appears that this treatment modality does not act on reflexive responses exclusively. Other mechanisms, such as viscoelastic features and mechanical factors, are probably also involved. The combined measurement of torque and electromyographic activity in stretched muscle groups during passive movements is a useful tool for identifying features and underlying mechanisms of spastic hypertonia in people with stroke.
Acknowledgements
We thank Kris Bogaerts from the Biostatistical Centre at the University of Leuven for his assistance in the statistical analysis of the data.
References
- Duncan, P, Richards, L, Wallace, D et al. A randomized, controlled pilot study of a home-based exercise program for individuals with mild and moderate stroke. Stroke. 1998; 29: 2055–2060
- Feys, HM, De Weerdt, WJ, Selz, BE et al. Effect of a therapeutic intervention for the upper limb in the acute phase after stroke: a single-blind, randomized, controlled multicenter trial. Stroke. 1998; 29: 785–792
- Katz, RT. Management of spastic hypertonia after stroke. J Neuro Rehabil. 1991; 5: 5–12
- Partridge, C. Physiotherapy approaches to the treatment of neurological conditions: an historical perspective.in: Neurological physiotherapy: a problem-solving approach. : Churchill Livingstone, New York; 1996: 3–14
- Davies, JM, Mayston, MJ, and Newham, DJ. Electrical and mechanical output of the knee muscles during isometric and isokinetic activity in stroke and healthy adults. Disabil Rehabil. 1996; 18: 83–90
- Lamontagne, A, Malouin, F, Richards, CL, and Dumas, F. Evaluation of reflex- and nonreflex-induced muscle resistance to stretch in adults with spinal cord injury using hand-held and isokinetic dynamometry. Phys Ther.1998; 78: 964–978
- Walsh, EG. Muscles, masses and motion. The physiology of normality, hypotonicity, spasticity and rigidity. : Blackwell Scientific, Oxford; 1992
- Dietz, V, Quintern, J, and Berger, W. Electrophysiological studies of gait in spasticity and rigidity. Evidence that altered mechanical properties of muscle contribute to hypertonia. Brain. 1981; 104: 431–449
- Dietz, V. Role of peripheral afferents and spinal reflexes in normal and impaired human locomotion. Rev Neurol (Paris). 1987; 143: 241–254
- O'Dwyer, NJ, Ada, L, and Neilson, PD. Spasticity and muscle contracture following stroke. Brain. 1996; 119:1737–1749
- Lance, JW. Symposium synopsis. in: Spasticity: disordered motor control. : Year Book Publishers, Chicago;1980: 51
- Greenberg, DA, Aminoff, MJ, and Simon, RP. Clinical neurology. : Prentice Hall, London; 1993
- Knutsson, E and Måartensson, A. Dynamic motor capacity in spastic paresis and its relation to prime mover dysfunction, spastic reflexes and antagonist co-activation. Scand J Rehabil Med. 1980; 12: 93–106
- Thilmann, AF, Fellows, SJ, and Garms, E. The mechanism of spastic muscle hypertonus. Variation in reflex gain over the time course of spasticity. Brain. 1991; 114: 233–244
- Given, JD, Dewald, JPA, and Rymer, WZ. Joint dependent passive stiffness in paretic and contralateral limbs of spastic patients with hemiparetic stroke. J Neurol Neurosurg Psychiatry. 1995; 59: 271–279
- Perry, J. Determinants of muscle function in the spastic lower extremity. Clin Orthop. 1993; 288: 10–26
- Brown, RA, Lawson, DA, Leslie, GC et al. Does the Wartenberg pendulum test differentiate quantitatively between spasticity and rigidity? A study in elderly stroke and Parkinsonian patients. J Neurol Neurosurg Psychiatry. 1988; 51: 1178–1186
- Ashworth, B. Preliminary trial of carisoprodol in multiple sclerosis. Practitioner. 1964; 192: 540–542
- Basmajian, JV and Blumenstein, R. Electrode placement in EMG biofeedback. : Williams & Wilkins, Baltimore;1980
- Spaepen, A, Baumann, W, and Maes, H. Relation between mechanical load and EMG-activity of selected muscles of the trunk underisometric conditions. in: Biomechanics: basic and applied research. Selected proceedings of the 5th Meeting of the European Society of Biomechanics; 1986 Sep 8-10; Berlin (Germany). : Martinus Nijhoff, Dordrecht; 1987: 595–600
- Verbeke, G and Molenberghs, G. Linear mixed models in practice: a SAS-oriented Approach. : Springer, New York; 1997
- Davidoff, RA. Skeletal muscle tone and the misunderstood stretch reflex. Neurology. 1992; 42: 951–963
- McHugh, MP, Kremenic, IJ, Fox, MB, and Gleim, GW. The role of mechanical and neural restraints to joint range of motion during passive stretch. Med Sci Sports Exerc. 1998; 30: 928–932
- Berger, W, Horstmann, GA, and Dietz, V. Spastic paresis: impaired spinal reflexes and intact motor programs.J Neurol Neurosurg Psychiatry. 1988; 51: 568–571
- Dietz, V, Trippel, M, and Berger, W. Reflex activity and muscle tone during elbow movements in patients with spastic paresis. Ann Neurol. 1991; 30: 767–779
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