Journal of Bodywork & Movement Therapies (2015) 19, 284e290
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PROSPECTIVE STUDY: MUSCLE PHYSIOLOGY IN STROKE PATIENTS
The relationship between isokinetic muscle strength and spasticity in the lower limbs of stroke patients I. Abdollahi, PhD, PT a, A. Taghizadeh, MSc, PT a, H. Shakeri, PhD, PT a, M. Eivazi, PhD, PT b, S. Jaberzadeh, PhD, PT c,* a
Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran Department of Physiotherapy, Tabriz Medical Sciences University, Tabriz, Iran c Department of Physiotherapy, School of Primary Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Australia b
Received 13 January 2013; received in revised form 8 July 2014; accepted 10 July 2014
KEYWORDS Stroke; Spasticity; Muscle strength; Isokinetic
Summary Objective: In this study the relationship between degree of spasticity and strength of knee extensor and ankle plantar flexor muscles of post stroke hemiparetic patients has been investigated. Materials & methods: The participants of this study were 40 stroke patients whose elapsed time of stroke onset was at least 3 months. Their age averaged 59 years. Spasticity was measured with the Modified Ashworth Scale. Isokinetic muscle strength was measured with an isokinetic dynamometer. Two methods of torque normalization e subtractive and weight based normalization e were used for comparing torques among participants. Results: Kendall’s tau-b coefficient was calculated for investigating this relationship. This coefficient was not significant for the relationship between weight based normalized data and modified Ashworth scale (MAS) in any of each muscle groups (a Z 0.05). This coefficient was significant for the relationship between the subtractive normalization method and MAS in knee extensors (P Z 0.005, a Z 0.01) and ankle plantar flexors (P Z 0.002, a Z 0.01). Conclusion: This study suggests a negative relationship between spasticity and muscle strength and provided evidence that spastic muscles are weaker. ª 2014 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ61 3 9904 4827, þ61 0433345789 (mobile); fax: þ61 3 9904 4812. E-mail address: [email protected] (S.Jaberzadeh). http://dx.doi.org/10.1016/j.jbmt.2014.07.002 1360-8592/ª 2014 Elsevier Ltd. All rights reserved.
Management of spasticity in stroke patients
Introduction Cardiovascular accidents (CVA) such as stroke are considered the third most common cause of death and long-term disability in western countries (Ada et al., 2006). In Iran the prevalence of ischemic stroke among Iranian young adults (15e45 years) has been recorded as 8 per 100,000 head of population (Ghandehari and Izadi Moud, 2006). According to a study carried out in Babol (2001e2003), a northern city of Iran, stroke incidence was reported to be 50 per 100,000 (Ahangar et al., 2005). In addition to long-term disability, stroke causes significant psychological problems for patients and their families. On a worldwide scale it is predicted that by 2020, stroke and heart coronary disease would have become the primary causes of death and longterm disabilities in both western (WHO, 2000; Foulkes et al., 1988) and other countries such as IRAN. One aspect of stroke and coronary heart disease is lesions in the pyramidal and extrapyramidal pathways. These may be followed by positive and negative symptoms. Spasticity, clonus, associated reactions and abnormal postures are considered as positive symptoms. Negative symptoms include muscle weakness, muscle fatigue and lack of muscle precision (Bente and Bassoe, 2008). The most important negative sign in stroke patients is paralysis or weakness of muscles of the contralateral limbs, the trunk, and sometimes half of the face (Fredericks and Saladin, 1996). In contrast to this, one of the most important positive signs after stroke is spasticity. The pathophysiology of spasticity is still unclear. It has long been thought that the increased gain of stretch reflexes in spasticity resulted from hyperactivity of the gamma motor neurons. Recent studies indicate that while gamma motor activity may be present in some cases, changes in the background activity of alpha motor neurons and interneurons is probably a more important factor in spasticity (Fredericks and Saladin, 1996). Muscle weakness, paralysis and spasticity on the affected side are common symptoms in stroke patients (Andrews et al., 1982; Fugl-Meyer et al., 1975). Literature on the subject indicates that stroke patients with spasticity experience more functional problems than patients without spasticity (Watkins et al., 2002), and research has shown a significant correlation between the affected limb muscle strength and functional outcomes (Hsu et al., 2002). Various therapeutic methods have been developed to reduce the impact of spasticity on physical performance. Bobath, who considered muscle spasticity as a major disorder, emphasized the use of inhibitory methods such as handling and reflex inhibitory patterns (RIP) (Bobath, 1990). In contrast, Carr and Shepherd considered muscle weakness as the most important issue. Their method of responding to spasticity is to use motor relearning programs (MRPs) as the pivotal method for strengthening weak muscles in patients suffering stroke (Carr and Shepherd, 1989). Both these methods have their followers, but the superiority of one over the other has not yet been established. Langhammer, 2000, conducted a double-blind study and compared the effects of the two approaches to stroke rehabilitation mentioned above e the Bobath method and
285 Carr and Shepherd’s MRPs e on two groups of 33 and 28 stroke patients. Data were collected before, and at three days, two weeks and three months post intervention. In spite of modest differences between these two approaches at two weeks, the result of this study indicated no difference in the outcomes of these approaches at three days and three months post intervention, thus failing to indicate the superiority of one method over the other. The same investigator performed a follow-up study in 2003 and this time examined the effects of both treatment methods on participants after one and four years. These follow-up measurements also failed to show any significant differences between the two therapeutic approaches (Langhammer, 2003), leaving the question of the superiority of one approach over the other remaining unanswered. Since the behavior of spastic muscles in stroke survivors has not been fully understood, any research in this area may shed light on the relationship between spasticity and muscle strength. Any positive relationship between spasticity and muscle strength would indicate that spastic muscles are strong, and therefore muscle weakness is not be the main problem would indicate the preferred treatment would tend to be the Bobath inhibitory methods. On the other hand, if the relationship between spasticity and muscle strength proves to be negative, indicating that spastic muscles are weak, then treatment methods would focus on facilitatory movement such as in motor relearning programs. Recognition of the behavior of spastic muscles could be very important in determining the superiority of treatment methods. Moreover, to understand the behavior of spastic muscles it could be possible to make a decision about the potential impact of spasticity on the muscle strength. Studies have evaluated the effects of the strengthening and progressive resistance of isokinetic exercise on spastic muscle tone and strength in lower extremities. Some of these studies have shown that strength increased without changing muscle tone (Flansbjer et al., 2008; Badics et al., 2002; Shelly and Brenda, 1997). In 1987, Bohannon et al., (1987) also studied the effects of the strengthening and progressive resistance of isokinetic exercise on spastic muscle tone and strength, but in relation to upper limbs. They found a significant correlation between the spasticity and strength of the involved muscles. The main aim of the current study is to investigate the correlation between degree of spasticity and isokinetic muscle strength in the lower extremities in unilateral stroke patients. To our knowledge, this is the first study investigating this relationship. We have hypothesized that, in lower extremity muscles in unilateral stroke patients, there is an inverse relationship between degree of spasticity and isokinetic muscle strength.
Materials and methods In this non-experimental prospective study that performed in Rofaydeh Rehabilitation Hospital, 40 stroke patients (22 male and 18 female) were selected from hospitals and rehabilitation centers in Tehran in a simple non-probability sampling method. 21 participants had right side
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I. Abdollahi et al. extensor muscles was based on a report by Brunnstrom indicating involvement of extensor muscles in 95% of stroke survivors (Brunnstrom, 1970). In all participants the spasticity test was performed before strength testing to avoid the possible effects of strength testing on muscle tone, and at the same time preventing the bias that might result from the testing of isokinetic strength before tone. There was a 30 min time interval between the spasticity measurement and strength testing.
Reliability study
Figure 1 Assessment of knee extensor spasticity by Modified Ashworth Scale in side lying position.
involvement, and in all participants the right side was dominant. The average elapsed time after stroke was 15.87 months. The inclusion criteria were the history of ischemic hemiparetic stroke with at least three months duration past history, the ability to walk at least 12 m with or without assistive devices, and having a maximum spasticity score of two from the Modified Ashworth scale (MAS). Patients excluded were those with a history of: more than one stroke, severe artery involvement in the sub dura mater, disorders like multiple sclerosis or Parkinson’s Disease with their dramatic effects on muscle tone and strength, severe pain, cognitive disorders, heart failure, high blood pressure and unstable angina. These criteria were tested against a neurological diagnosis, medical records and a clinical examination by researchers (registered physiotherapists). In this study two types of data, maximum isokinetic torque (MIT) and degree of spasticity (DOS) were collected. The MIT of knee extensors and ankle plantar flexors from normal and involved lower extremities was recorded using a Cybex isokinetic machine Model 770 (Fig. 1). The Modified Ashworth Scale was utilized to quantify DOS in these muscles. The reason for the selection of these
Before performing the main study, the intersession reliability of the muscle strength (torque) and spasticity measurements were assessed in a separate study. Strength of knee extensors and ankle plantar flexors was evaluated on 8 patients (4 woman, 4 men) on two separate occasions, one week apart, using an isokinetic device (Blackburn et al., 2002). The reliability of two methods of torque normalization e subtractive and weight-based normalization (refer to main study, page 9, for further detail) e was tested in this reliability study. The inter-session reliability of the measured muscle strength was assessed using intraclass correlation coefficient (ICC). ICC values and their 95% confidence intervals (CI) are presented in Table 1. Systematic bias was also evaluated by measuring the level of agreement using paired t-test to compare the values for day 1 and 2 measurements. This test revealed no significant time effect for any of these two normalisation methods (Table 1). Spasticity of affected knee extensors and ankle plantar flexors was evaluated on 15 patients (6 woman, 9 men) on two separate occasions, one week apart, employing procedures used by Blackburn et al. (2002) and Allison et al. (1996) respectively. The inter-session reliability of the measured spasticity was assessed using Kendall tau-b correlation Index. This is a nonparametric statistical test, used to measure the association and also agreement between the measurements at day 1 and 2 (Table 1). The index must be in the range 1 KTau-b þ1. If the agreement between the two rankings is perfect (i.e., the two rankings are the same) the coefficient has value þ1. If
Table 1 Mean and ICC values and their 95% confidence intervals (CI) for isokinetic torque. Kendall tau-b correlation Index and agreement for spasticity.
Isokinetic torque Knee extension Subtractive method Weight normalization Ankle dorsiflexion Subtractive method Weight normalization
Spasticity Knee extensor muscles Ankle plantar flexors
n
Mean Day1eDay2
ICC (95% CI-upper-lower)
Paired t-test Day1eDay2
8 8
0.386e0.437 0.710e0.896
0.863 (0.314e0.973) 0.937 (0.684e0.987)
P Z 0.17 P Z 0.11
8 8
0.378e0.400 0.688e0.780
0.704 (0.480e0.941) 0.799 (0.005e0.960)
P Z 0.14 P Z 0.09
n
Kendall tau-b correlation Index (Association between the two rankings at Day1 and Day2)
Agreement between the two rankings at Day1 and Day2
15 15
0.789 0.663
w79% w66%
Management of spasticity in stroke patients
287
the disagreement between the two rankings is perfect (i.e., one ranking is the reverse of the other) the coefficient has value 1. In this reliability study both indexes for knee extensor and ankle flexor spasticity were positive, which indicate moderate (66% for ankle plantar flexors) to strong (79% for knee extensors) agreement between the rankings at Day1 and Day2 (Table 1).
Main study After placing the patients on the plinth, they were given 5 min rest to relax their muscles. The first muscle group for spasticity testing was selected randomly. Muscle tone was recorded by one of the researchers by testing three consecutive movements, each lasting about 1 s. To test knee extensor muscle tonicity, the patient was kept in a side-lying position so that the test side was positioned above the other side. The knee and hip were positioned in extension. The examiner stood behind the patient and put one hand above the knee for stabilization, and the other one above the ankle to move the knee from full extension to full flexion (Fig. 1). To test plantar flexor muscle spasticity the patient sat on a chair so that hip and knee joints were positioned in 80 and 60 flexion. The examiner was positioned in front of the patient with one hand underneath the foot with their thumb placed on the medial aspect of the heel, and their forearm making contact with the plantar surface of the foot. The examiner then asked the patient to relax as much as possible, and proceeded to move the ankle from full plantar flexion to full dorsiflexion (Fig. 2). After evaluation of the muscle tone, the maximum isokinetic torque of knee extensor and ankle plantar flexor muscles in the affected and non-affected sides was recorded based on the method suggested by Hsu et al. (2002). All measurements were conducted first on the non-affected side, and then the affected side, to enable familiarity with the testing procedure. The muscle group to be tested first was selected randomly. Each test involved three warmup trials followed by 5 min of rest and then 4 test contractions. To test knee extensor muscles, the angle of
inclination of the back-seat of the isokinetic machine was set at 30 to the horizontal plane. The patient’s knee hung over the edge of the chair and a pad was placed proximal to the ankle. A velocity of 90 /sec was used for the knee extensor muscle strength test (Fig. 3). To test plantar flexor muscles the back of the seat was placed in a horizontal position and the ankle was secured. Its velocity was set at 30 /s (Fig. 4). These speeds were selected because the previous research of others had indicated a strong data reliability at these speeds Hsu et al. (2002). Audio and visual feedback/encouragement was used to obtain maximum torque in participants. Since muscle strength is dependent on many factors such as genetics, age, sex, weight, for comparative purposes two methods were used to calculate the strength output of the affected limbs by an isokinetic device. In the first method, the weight based normalization method (WBNM), the measured strength of the muscle is divided by the patient’s body weight. In the second method, the subtractive normalization method (SNM), the difference between the
Figure 2 Assessment of ankle plantar flexor spasticity by Modified Ashworth Scale in supine position.
Figure 4 Setting of isokinetic device used for measurement of isokinetic torque of plantar flexors.
Figure 3 Isokinetic device used for measurement of isokinetic torque of knee extensors. The axis of the knee joint was aligned with axis of device.
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average maximum isokinetic torque of the non-affected side and that of the affected side is divided by the strength of the non-affected isokinetic torque. SPSS version 16 was utilized for statistical analysis. The limit for statistical significance was set at P Z 0.05.
Results Demographic data and isokinetic knee and ankle torque, using both methods of normalization, WBNM and SNM, are summarized in Table 2. A comparison of normalized isokinetic data, based on SNM in the knee extensor muscle and ankle plantar flexor groups, indicates that the subtractive data range in the ankle plantar flexor muscles (Kendal tau-b Z 0.380 and P Z 0.002) is somewhat greater than in the knee extensor muscles (Kendal tau-b Z 0.359 and P Z 0.005) (Table 3). The presence of negative values in the subtractive method of normalization (Table 2) shows that in a number of patients the torque of the involved side was higher than the non-involved side. Table 3 demonstrates the isokinetic normalized data based on the WBNM in the knee extensor and ankle plantar flexor groups. No negative values were obtained using this normalization method. For each muscle group two ranking data were obtained by using the Modified Ashworth Scale. A comparison of the frequency and distribution of the knee extensors and ankle plantar flexors in the involved side indicates that dispersion of muscle spasticity in the ankle plantar flexors in the patients with left side involvement was higher than knee extensor muscles. We calculated the Kendall Tau-b coefficient using a twotailed test to determine the correlation between normalized isokinetic torques and the ordinal data (obtained from the modified Ashworth scale) from knee extensor and ankle plantar flexor muscles. This coefficient was 0.204 for knee extensors (P Z 0.109) and 0.153 for plantar flexors (P Z 0.217) using the weight based normalized method. This does not reject the null hypothesis, therefore the variables are uncorrelated at a 0.05 significance level. The Kendall Tau-b correlation between the subtractive normalized isokinetic torque and the nominal data from measurements of the MAS of the knee extensor and ankle plantar flexor muscle group was 0.359 (P Z 0.005) and 0.380 (P Z 0.002) respectively. These data rejects the null
Table 2 Main descriptive data in stroke patients with two normalization methods. Variable
Population Mean SD
Age Weight Time elapsed Isokinetic knee torque Substractive method Weight normalization Isokinetic plantar flexor torque Subtractive method Weight normalization
40 40 40 40
40
Measure
59.32 14.32 year 67.69 11.84 kg 15.87 16.20 month n.m/n.m 0.33 0.23 1.12 0.53 n.m/n.m 0.26 0.76
0.24 0.34
Table 3 Kendal’s tau-b coefficients and P values for both isokinetic knee torque and isokinetic plantar flexor torque. Variable
Isokinetic knee torque Substractive method Weight normalization Isokinetic plantar flexor torque Substractive method Weight normalization
Kendal’s tau-b coefficient
P value
a
Significant
0.05 0.359
0.005
Yes
0.204
0.109
No 0.05
0.380
0.002
Yes
0.153
0.217
No
hypothesis that variables are uncorrelated at the 0.05 significance level. An Index of 0.359 and 0.380 indicates a weak correlation between data obtained directly from the subtractive method of normalizing and data measuring degree of spasticity. In fact it indicates that with an increasing severity of spasticity there was an increase in this index, and with its decrement the index was decreased.
Discussion Unlike when using the weight method, the relationship between the data group that normalized by the subtractive method in both ankle plantar flexor and knee extensor muscles with severe spasticity was statistically significant. This finding could be explained by the lack of a linear relationship between muscle mass and body weight, which tallies with previous studies. Janssen et al. (2000) showed the presence of a significant linear relationship between height and age and muscle mass, whereas the relationship between weight and muscle mass is not linear. As a whole, it seems that using weight for data normalizing is not an appropriate criterion. However, the correlation between normalized isokinetics data, based on the subtractive method, and MAS data indicates a relationship that is useful and reliable. Kendall’s Tau-b coefficient based on subtractive data in plantar flexor muscles was higher than in knee extensors, probably because of the greater variation in data obtained from MAS and higher data range in ankle plantar flexor muscles. As indicated in Figs. 4 and 5, the range of MAS in the ankle plantar flexors in the involved sides ranged from 0 to þ2, while the range of MAS in the knee extensor muscles ranged from 0 to þ1. This diversity increases the correlation coefficient in the plantar flexor muscles. As can be seen in Table 3, some of the data points obtained by the subtractive normalizing method showed negative values. In the subtractive normalizing method, where we made subtracted the measurements of the involved side from those of the uninvolved side, and divided this by the torque of the normal side to calculate
Management of spasticity in stroke patients
289 (2002), was not as common as weakness, their effect of spasticity on disability and performance of stroke patients should not be ignored. Spasticity, apart from its negative effects on patients performance, could give rise to muscle contracture (Botte et al., 1988; Harburn and Potter, 1993).
Clinical implications
Figure 5 Frequency and dispersion of Modified Ashworth Scale scores of knee extensor muscle depending on involved side (X axis is spastic muscle and Y axis is subject population).
normalized values, the presence of negative values indicate that in these patients the torque of the involved side was higher than the non-involved side. The relative weakness of the uninvolved side in some stroke patients is consistent with the results of Harris et al. (2001) that concluded weakness develops in the noninvolved side’s quadriceps muscle in stroke patients. Harris and colleagues evaluated the patients in the first week after stroke, while we studied patients at least three months after the stroke event. One possible explanation for this is that some patients may have exerted more effort with their affected side during the isokinetic strength test to show that it has enough strength. However, with comparable results in both studies it seems reasonable to assume that in these patients more attention should be given to the non-involved side. Having a significant direct relationship between spasticity severity and strength that normalized, based on the subtraction method, indicates a negative correlation between the degree of spasticity and strength, and in fact represents the weakness of muscles with more spastic tone in comparison with other muscles. Therefore, in treatment we should place more emphasis on muscles with severe spasticity. However, due to the non-experimental nature of this study, it is not possible to conclude this result directly from this research. A negative significant relationship between degree of spasticity and muscle strength in the lower extremities indicates that spasticity has a negative impact on muscle strength. Therefore, patients with severe spasticity may have weaker muscles, and treatment methods in these stroke patients tend to focus on motor retraining programs. It is not possible to ignore the significant negative effects of spasticity on the function of stroke patients. Probably it seems that spasticity, as an abnormal tone, blocks the development of voluntary muscle tone and obstructs the contractile capacity of the voluntary contraction in muscle. Leathley et al. (2004) demonstrated that if the Barthel index score 7 days after stroke is low, or early muscle weakness is high, we can expect more chance of severe spasticity later. Occurrences of severe spasticity with severe muscle weakness typically presents the possibility that spasticity and strength compete with each other in taking control of muscle contractile capacity. Although the prevalence of spasticity, about 38% as reported by Watkins et al.
The results of this study indicate that, in spastic stroke patients, spasticity management techniques could be used before the application of strengthening techniques. This points to a combination of these two approaches being more useful than the individual application of these treatment methods. As spasticity management may help muscle strength development in its primary stages, it is recommended that the combined treatment procedure should be used in treatment of spastic stroke patients.
Limitations of the study In patients with severe muscle weakness or severe spasticity, it was not possible to test isokinetic muscle strength. So, patients with weak muscles or severe spasticity (measuring 3 or more on the modified Ashworth Scale) were excluded from this study. This has been an observational study, which at most gives us the relationship between the studied variables. Therefore in this study we cannot form conclusions about the causes of changes or relationships. Further studies are required to address these causes.
Suggestions for future research We suggest that research could be conducted to measure the effect of spasticity decrease on spastic muscle strength. And the effect of inhibitory procedures such as reflex inhibitory patterns (RIP) and stretching methods on the muscle tone and strength of spastic muscles in stroke patients could be examined.
Conclusion In this study we found a relationship between severity of spasticity and muscle strength that normalized, based on the subtraction method. The results indicate that there is an opposite relationship between the degree of muscle spasticity and isokinetic muscle strength. This finding indicates that spastic muscles are weaker and the focus of treatment should be on spastic muscles.
Acknowledgments The authors thank physiotherapy staffs of Tabassom rehabilitation center, Baharloo, 7th Tir, Loghman, Alghadir and Ziaian hospitals and physiotherapy department of Social Welfare and Rehabilitation Sciences for supporting this research.
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References Ada, L., Dorsch, S., Canning, C.G., 2006. Strengthening interventions increase strength and improve activity after stroke: a systematic review. Aust. J. Physiother. 52, 241e248. Ahangar, A.A., Vaghefi, S.B.A., Ramaezani, M., 2005. Epidemiological evaluation of stroke in Babol, Northern Iran (2001e2003). Eur. Neurol. 54, 93e97. Allison, S.C., Abraham, L.D., Petersen, C.L., 1996. Reliability of Modified Ashworth Scale in the assessment of PlantarFlexor muscle spasticity in patients with traumatic brain injury. Int. J. Rehabil. Res. 19, 67e78. Andrews, K., Blocklehurst, J.C., Richards, B., et al., 1982. The recovery of the severely disabled stroke patient. Rheumatol. Rehabil. 21, 225e230. Badics, E., Rupp, M., Stabauer, B., Zifko, U.A., Wittmann, A., 2002. Systematic muscle building exercises in the rehabilitation of stroke patients. NeuroRehabilitation 17, 211e214. Bente, E., Bassoe, G., 2008. The Bobath Concept in Adult Neurology. Thieme. Blackburn, M., Villet, p, Mocket, S.P., 2002. Reliability of measurements obtained with the modified ashworth scale in the lower extremities of people with stroke. Phys. Ther. 82, 25e34. Bobath, B., 1990. Hemiplegia: Evaluation and Treatment. Heinmann Medical Books. Bohannon, R.W., Larkin, P.A., Smith, M.B., Horton, M.G., 1987. Relationship between static muscle strength deficits and spasticity in stroke patients with hemiparesis. Phys. Ther. 67, 1067e1071. Botte, M.J., Nickel, V.L., Akeson, W.H., 1988. Spasticity and contractures: physiologic aspects of formation. Orthop. Relat. Res. 233, 7e18. Brunnstrom, S., 1970. Movement Therapy in Hemiplegia: a Neurophysiological Approach. Medical Dept., Harper & Row, p. 192. Carr, T.H., Shepherd, R.B., 1989. A Motor Learning Program for Stroke. Heinmann, London. Flansbjer, U.B., Miller, M., Downham, D., Lexell, J., 2008. Progressive resistance training after stroke: effects on muscle strength, muscle tone, gait performance and perceived participation. J. Rehabil. Med. 40, 42e48.
I. Abdollahi et al. Foulkes, A., Wolf, P.A., Mohr, J.P., Hier, D.B., 1988. The stroke data bank: design, methods, and baseline characteristics. Stroke 19, 547e554. Fredericks, C.M., Saladin, L.K., 1996. Phatophysiology of the Motor Systems: Principles and Clinical Presentations. FA Davis, Philadelphia. Fugl-Meyer, A.R., Jassko, L., Leyman, L., 1975. The post-stroke hemiplegic patient: a method for evaluation of physical performance. Scand. J. Rehabil. Med. 7, 13e31. Ghandehari, K., Izadi Moud, Z., 2006. Incidence and etiology of ischemic stroke in Persian young adults. Acta Neurol. Scand. 113, 121e124. Harburn, K.L., Potter, P.J., 1993. Spasticity and contractures. Phys. Med. Rehabil. 7, 113e132. Harris, M.L., Bath, P.M.W., Moxham, J., 2001. Quadriceps muscle meakness following acute hemoplegic stroke. Clin. Rehabil. 15, 274e281. Hsu, A.L., Jan, M.H., Tang, P.F., 2002. Test-retest reliability of isokinetic muscle strength of the lower extremities in patients with stroke. Arch. Phys. Med. Rehabil. 83, 1130e1137. Janssen, I., Heymsfield, S.B., Wang, Z., Ross, R., 2000. Skeletal muscle mass and distribution in 468 men and women aged 18_88 yr. J. Appl. Physiol. 89, 81e88. Langhammer, B., 2003. Bobath or motor relearning programme? A follow-up one and four years post stroke. Clin. Rehabil. 17, 731e734. Langhammer, B., 2000. Bobath or motor relearning programme? A comparison of two different approaches of physiotherapy in stroke rehabilitation: a randomized controlled study. Clin. Rehabil. 14, 361e369. Leathley, M.J., Gregson, J.M., Moore, A.P., Smith, T.L., Sharma, A.K., Watkins, C.L., 2004. Predicting spasticity after stroke in those surviving to 12 months. Clin. Rehabil. 18, 438e443. Shelly, A.S., Brenda, J.B., 1997. Isokinetic strength training of the hemiparetic knee: effects on function and spasticity. Arch. Phys. Med. Rehabil. 78, 1231e1236. Watkins, C.L., Leathley, M.J., Gregson, J.G., Moore, A.P., Smith, T.H., Sharma, A.K., 2002. Prevalence of spasticity post stroke. Clin. Rehabil. 16, 515e522. WHO the World Health Report, 2000. WHO, Genera.
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ScienceDirect journal homepage: www.elsevier.com/jbmt
PROSPECTIVE STUDY: MUSCLE PHYSIOLOGY IN STROKE PATIENTS
The relationship between isokinetic muscle strength and spasticity in the lower limbs of stroke patients I. Abdollahi, PhD, PT a, A. Taghizadeh, MSc, PT a, H. Shakeri, PhD, PT a, M. Eivazi, PhD, PT b, S. Jaberzadeh, PhD, PT c,* a
Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran Department of Physiotherapy, Tabriz Medical Sciences University, Tabriz, Iran c Department of Physiotherapy, School of Primary Health Care, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Australia b
Received 13 January 2013; received in revised form 8 July 2014; accepted 10 July 2014
KEYWORDS Stroke; Spasticity; Muscle strength; Isokinetic
Summary Objective: In this study the relationship between degree of spasticity and strength of knee extensor and ankle plantar flexor muscles of post stroke hemiparetic patients has been investigated. Materials & methods: The participants of this study were 40 stroke patients whose elapsed time of stroke onset was at least 3 months. Their age averaged 59 years. Spasticity was measured with the Modified Ashworth Scale. Isokinetic muscle strength was measured with an isokinetic dynamometer. Two methods of torque normalization e subtractive and weight based normalization e were used for comparing torques among participants. Results: Kendall’s tau-b coefficient was calculated for investigating this relationship. This coefficient was not significant for the relationship between weight based normalized data and modified Ashworth scale (MAS) in any of each muscle groups (a Z 0.05). This coefficient was significant for the relationship between the subtractive normalization method and MAS in knee extensors (P Z 0.005, a Z 0.01) and ankle plantar flexors (P Z 0.002, a Z 0.01). Conclusion: This study suggests a negative relationship between spasticity and muscle strength and provided evidence that spastic muscles are weaker. ª 2014 Elsevier Ltd. All rights reserved.
* Corresponding author. Tel.: þ61 3 9904 4827, þ61 0433345789 (mobile); fax: þ61 3 9904 4812. E-mail address: [email protected] (S.Jaberzadeh). http://dx.doi.org/10.1016/j.jbmt.2014.07.002 1360-8592/ª 2014 Elsevier Ltd. All rights reserved.
Management of spasticity in stroke patients
Introduction Cardiovascular accidents (CVA) such as stroke are considered the third most common cause of death and long-term disability in western countries (Ada et al., 2006). In Iran the prevalence of ischemic stroke among Iranian young adults (15e45 years) has been recorded as 8 per 100,000 head of population (Ghandehari and Izadi Moud, 2006). According to a study carried out in Babol (2001e2003), a northern city of Iran, stroke incidence was reported to be 50 per 100,000 (Ahangar et al., 2005). In addition to long-term disability, stroke causes significant psychological problems for patients and their families. On a worldwide scale it is predicted that by 2020, stroke and heart coronary disease would have become the primary causes of death and longterm disabilities in both western (WHO, 2000; Foulkes et al., 1988) and other countries such as IRAN. One aspect of stroke and coronary heart disease is lesions in the pyramidal and extrapyramidal pathways. These may be followed by positive and negative symptoms. Spasticity, clonus, associated reactions and abnormal postures are considered as positive symptoms. Negative symptoms include muscle weakness, muscle fatigue and lack of muscle precision (Bente and Bassoe, 2008). The most important negative sign in stroke patients is paralysis or weakness of muscles of the contralateral limbs, the trunk, and sometimes half of the face (Fredericks and Saladin, 1996). In contrast to this, one of the most important positive signs after stroke is spasticity. The pathophysiology of spasticity is still unclear. It has long been thought that the increased gain of stretch reflexes in spasticity resulted from hyperactivity of the gamma motor neurons. Recent studies indicate that while gamma motor activity may be present in some cases, changes in the background activity of alpha motor neurons and interneurons is probably a more important factor in spasticity (Fredericks and Saladin, 1996). Muscle weakness, paralysis and spasticity on the affected side are common symptoms in stroke patients (Andrews et al., 1982; Fugl-Meyer et al., 1975). Literature on the subject indicates that stroke patients with spasticity experience more functional problems than patients without spasticity (Watkins et al., 2002), and research has shown a significant correlation between the affected limb muscle strength and functional outcomes (Hsu et al., 2002). Various therapeutic methods have been developed to reduce the impact of spasticity on physical performance. Bobath, who considered muscle spasticity as a major disorder, emphasized the use of inhibitory methods such as handling and reflex inhibitory patterns (RIP) (Bobath, 1990). In contrast, Carr and Shepherd considered muscle weakness as the most important issue. Their method of responding to spasticity is to use motor relearning programs (MRPs) as the pivotal method for strengthening weak muscles in patients suffering stroke (Carr and Shepherd, 1989). Both these methods have their followers, but the superiority of one over the other has not yet been established. Langhammer, 2000, conducted a double-blind study and compared the effects of the two approaches to stroke rehabilitation mentioned above e the Bobath method and
285 Carr and Shepherd’s MRPs e on two groups of 33 and 28 stroke patients. Data were collected before, and at three days, two weeks and three months post intervention. In spite of modest differences between these two approaches at two weeks, the result of this study indicated no difference in the outcomes of these approaches at three days and three months post intervention, thus failing to indicate the superiority of one method over the other. The same investigator performed a follow-up study in 2003 and this time examined the effects of both treatment methods on participants after one and four years. These follow-up measurements also failed to show any significant differences between the two therapeutic approaches (Langhammer, 2003), leaving the question of the superiority of one approach over the other remaining unanswered. Since the behavior of spastic muscles in stroke survivors has not been fully understood, any research in this area may shed light on the relationship between spasticity and muscle strength. Any positive relationship between spasticity and muscle strength would indicate that spastic muscles are strong, and therefore muscle weakness is not be the main problem would indicate the preferred treatment would tend to be the Bobath inhibitory methods. On the other hand, if the relationship between spasticity and muscle strength proves to be negative, indicating that spastic muscles are weak, then treatment methods would focus on facilitatory movement such as in motor relearning programs. Recognition of the behavior of spastic muscles could be very important in determining the superiority of treatment methods. Moreover, to understand the behavior of spastic muscles it could be possible to make a decision about the potential impact of spasticity on the muscle strength. Studies have evaluated the effects of the strengthening and progressive resistance of isokinetic exercise on spastic muscle tone and strength in lower extremities. Some of these studies have shown that strength increased without changing muscle tone (Flansbjer et al., 2008; Badics et al., 2002; Shelly and Brenda, 1997). In 1987, Bohannon et al., (1987) also studied the effects of the strengthening and progressive resistance of isokinetic exercise on spastic muscle tone and strength, but in relation to upper limbs. They found a significant correlation between the spasticity and strength of the involved muscles. The main aim of the current study is to investigate the correlation between degree of spasticity and isokinetic muscle strength in the lower extremities in unilateral stroke patients. To our knowledge, this is the first study investigating this relationship. We have hypothesized that, in lower extremity muscles in unilateral stroke patients, there is an inverse relationship between degree of spasticity and isokinetic muscle strength.
Materials and methods In this non-experimental prospective study that performed in Rofaydeh Rehabilitation Hospital, 40 stroke patients (22 male and 18 female) were selected from hospitals and rehabilitation centers in Tehran in a simple non-probability sampling method. 21 participants had right side
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I. Abdollahi et al. extensor muscles was based on a report by Brunnstrom indicating involvement of extensor muscles in 95% of stroke survivors (Brunnstrom, 1970). In all participants the spasticity test was performed before strength testing to avoid the possible effects of strength testing on muscle tone, and at the same time preventing the bias that might result from the testing of isokinetic strength before tone. There was a 30 min time interval between the spasticity measurement and strength testing.
Reliability study
Figure 1 Assessment of knee extensor spasticity by Modified Ashworth Scale in side lying position.
involvement, and in all participants the right side was dominant. The average elapsed time after stroke was 15.87 months. The inclusion criteria were the history of ischemic hemiparetic stroke with at least three months duration past history, the ability to walk at least 12 m with or without assistive devices, and having a maximum spasticity score of two from the Modified Ashworth scale (MAS). Patients excluded were those with a history of: more than one stroke, severe artery involvement in the sub dura mater, disorders like multiple sclerosis or Parkinson’s Disease with their dramatic effects on muscle tone and strength, severe pain, cognitive disorders, heart failure, high blood pressure and unstable angina. These criteria were tested against a neurological diagnosis, medical records and a clinical examination by researchers (registered physiotherapists). In this study two types of data, maximum isokinetic torque (MIT) and degree of spasticity (DOS) were collected. The MIT of knee extensors and ankle plantar flexors from normal and involved lower extremities was recorded using a Cybex isokinetic machine Model 770 (Fig. 1). The Modified Ashworth Scale was utilized to quantify DOS in these muscles. The reason for the selection of these
Before performing the main study, the intersession reliability of the muscle strength (torque) and spasticity measurements were assessed in a separate study. Strength of knee extensors and ankle plantar flexors was evaluated on 8 patients (4 woman, 4 men) on two separate occasions, one week apart, using an isokinetic device (Blackburn et al., 2002). The reliability of two methods of torque normalization e subtractive and weight-based normalization (refer to main study, page 9, for further detail) e was tested in this reliability study. The inter-session reliability of the measured muscle strength was assessed using intraclass correlation coefficient (ICC). ICC values and their 95% confidence intervals (CI) are presented in Table 1. Systematic bias was also evaluated by measuring the level of agreement using paired t-test to compare the values for day 1 and 2 measurements. This test revealed no significant time effect for any of these two normalisation methods (Table 1). Spasticity of affected knee extensors and ankle plantar flexors was evaluated on 15 patients (6 woman, 9 men) on two separate occasions, one week apart, employing procedures used by Blackburn et al. (2002) and Allison et al. (1996) respectively. The inter-session reliability of the measured spasticity was assessed using Kendall tau-b correlation Index. This is a nonparametric statistical test, used to measure the association and also agreement between the measurements at day 1 and 2 (Table 1). The index must be in the range 1 KTau-b þ1. If the agreement between the two rankings is perfect (i.e., the two rankings are the same) the coefficient has value þ1. If
Table 1 Mean and ICC values and their 95% confidence intervals (CI) for isokinetic torque. Kendall tau-b correlation Index and agreement for spasticity.
Isokinetic torque Knee extension Subtractive method Weight normalization Ankle dorsiflexion Subtractive method Weight normalization
Spasticity Knee extensor muscles Ankle plantar flexors
n
Mean Day1eDay2
ICC (95% CI-upper-lower)
Paired t-test Day1eDay2
8 8
0.386e0.437 0.710e0.896
0.863 (0.314e0.973) 0.937 (0.684e0.987)
P Z 0.17 P Z 0.11
8 8
0.378e0.400 0.688e0.780
0.704 (0.480e0.941) 0.799 (0.005e0.960)
P Z 0.14 P Z 0.09
n
Kendall tau-b correlation Index (Association between the two rankings at Day1 and Day2)
Agreement between the two rankings at Day1 and Day2
15 15
0.789 0.663
w79% w66%
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the disagreement between the two rankings is perfect (i.e., one ranking is the reverse of the other) the coefficient has value 1. In this reliability study both indexes for knee extensor and ankle flexor spasticity were positive, which indicate moderate (66% for ankle plantar flexors) to strong (79% for knee extensors) agreement between the rankings at Day1 and Day2 (Table 1).
Main study After placing the patients on the plinth, they were given 5 min rest to relax their muscles. The first muscle group for spasticity testing was selected randomly. Muscle tone was recorded by one of the researchers by testing three consecutive movements, each lasting about 1 s. To test knee extensor muscle tonicity, the patient was kept in a side-lying position so that the test side was positioned above the other side. The knee and hip were positioned in extension. The examiner stood behind the patient and put one hand above the knee for stabilization, and the other one above the ankle to move the knee from full extension to full flexion (Fig. 1). To test plantar flexor muscle spasticity the patient sat on a chair so that hip and knee joints were positioned in 80 and 60 flexion. The examiner was positioned in front of the patient with one hand underneath the foot with their thumb placed on the medial aspect of the heel, and their forearm making contact with the plantar surface of the foot. The examiner then asked the patient to relax as much as possible, and proceeded to move the ankle from full plantar flexion to full dorsiflexion (Fig. 2). After evaluation of the muscle tone, the maximum isokinetic torque of knee extensor and ankle plantar flexor muscles in the affected and non-affected sides was recorded based on the method suggested by Hsu et al. (2002). All measurements were conducted first on the non-affected side, and then the affected side, to enable familiarity with the testing procedure. The muscle group to be tested first was selected randomly. Each test involved three warmup trials followed by 5 min of rest and then 4 test contractions. To test knee extensor muscles, the angle of
inclination of the back-seat of the isokinetic machine was set at 30 to the horizontal plane. The patient’s knee hung over the edge of the chair and a pad was placed proximal to the ankle. A velocity of 90 /sec was used for the knee extensor muscle strength test (Fig. 3). To test plantar flexor muscles the back of the seat was placed in a horizontal position and the ankle was secured. Its velocity was set at 30 /s (Fig. 4). These speeds were selected because the previous research of others had indicated a strong data reliability at these speeds Hsu et al. (2002). Audio and visual feedback/encouragement was used to obtain maximum torque in participants. Since muscle strength is dependent on many factors such as genetics, age, sex, weight, for comparative purposes two methods were used to calculate the strength output of the affected limbs by an isokinetic device. In the first method, the weight based normalization method (WBNM), the measured strength of the muscle is divided by the patient’s body weight. In the second method, the subtractive normalization method (SNM), the difference between the
Figure 2 Assessment of ankle plantar flexor spasticity by Modified Ashworth Scale in supine position.
Figure 4 Setting of isokinetic device used for measurement of isokinetic torque of plantar flexors.
Figure 3 Isokinetic device used for measurement of isokinetic torque of knee extensors. The axis of the knee joint was aligned with axis of device.
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average maximum isokinetic torque of the non-affected side and that of the affected side is divided by the strength of the non-affected isokinetic torque. SPSS version 16 was utilized for statistical analysis. The limit for statistical significance was set at P Z 0.05.
Results Demographic data and isokinetic knee and ankle torque, using both methods of normalization, WBNM and SNM, are summarized in Table 2. A comparison of normalized isokinetic data, based on SNM in the knee extensor muscle and ankle plantar flexor groups, indicates that the subtractive data range in the ankle plantar flexor muscles (Kendal tau-b Z 0.380 and P Z 0.002) is somewhat greater than in the knee extensor muscles (Kendal tau-b Z 0.359 and P Z 0.005) (Table 3). The presence of negative values in the subtractive method of normalization (Table 2) shows that in a number of patients the torque of the involved side was higher than the non-involved side. Table 3 demonstrates the isokinetic normalized data based on the WBNM in the knee extensor and ankle plantar flexor groups. No negative values were obtained using this normalization method. For each muscle group two ranking data were obtained by using the Modified Ashworth Scale. A comparison of the frequency and distribution of the knee extensors and ankle plantar flexors in the involved side indicates that dispersion of muscle spasticity in the ankle plantar flexors in the patients with left side involvement was higher than knee extensor muscles. We calculated the Kendall Tau-b coefficient using a twotailed test to determine the correlation between normalized isokinetic torques and the ordinal data (obtained from the modified Ashworth scale) from knee extensor and ankle plantar flexor muscles. This coefficient was 0.204 for knee extensors (P Z 0.109) and 0.153 for plantar flexors (P Z 0.217) using the weight based normalized method. This does not reject the null hypothesis, therefore the variables are uncorrelated at a 0.05 significance level. The Kendall Tau-b correlation between the subtractive normalized isokinetic torque and the nominal data from measurements of the MAS of the knee extensor and ankle plantar flexor muscle group was 0.359 (P Z 0.005) and 0.380 (P Z 0.002) respectively. These data rejects the null
Table 2 Main descriptive data in stroke patients with two normalization methods. Variable
Population Mean SD
Age Weight Time elapsed Isokinetic knee torque Substractive method Weight normalization Isokinetic plantar flexor torque Subtractive method Weight normalization
40 40 40 40
40
Measure
59.32 14.32 year 67.69 11.84 kg 15.87 16.20 month n.m/n.m 0.33 0.23 1.12 0.53 n.m/n.m 0.26 0.76
0.24 0.34
Table 3 Kendal’s tau-b coefficients and P values for both isokinetic knee torque and isokinetic plantar flexor torque. Variable
Isokinetic knee torque Substractive method Weight normalization Isokinetic plantar flexor torque Substractive method Weight normalization
Kendal’s tau-b coefficient
P value
a
Significant
0.05 0.359
0.005
Yes
0.204
0.109
No 0.05
0.380
0.002
Yes
0.153
0.217
No
hypothesis that variables are uncorrelated at the 0.05 significance level. An Index of 0.359 and 0.380 indicates a weak correlation between data obtained directly from the subtractive method of normalizing and data measuring degree of spasticity. In fact it indicates that with an increasing severity of spasticity there was an increase in this index, and with its decrement the index was decreased.
Discussion Unlike when using the weight method, the relationship between the data group that normalized by the subtractive method in both ankle plantar flexor and knee extensor muscles with severe spasticity was statistically significant. This finding could be explained by the lack of a linear relationship between muscle mass and body weight, which tallies with previous studies. Janssen et al. (2000) showed the presence of a significant linear relationship between height and age and muscle mass, whereas the relationship between weight and muscle mass is not linear. As a whole, it seems that using weight for data normalizing is not an appropriate criterion. However, the correlation between normalized isokinetics data, based on the subtractive method, and MAS data indicates a relationship that is useful and reliable. Kendall’s Tau-b coefficient based on subtractive data in plantar flexor muscles was higher than in knee extensors, probably because of the greater variation in data obtained from MAS and higher data range in ankle plantar flexor muscles. As indicated in Figs. 4 and 5, the range of MAS in the ankle plantar flexors in the involved sides ranged from 0 to þ2, while the range of MAS in the knee extensor muscles ranged from 0 to þ1. This diversity increases the correlation coefficient in the plantar flexor muscles. As can be seen in Table 3, some of the data points obtained by the subtractive normalizing method showed negative values. In the subtractive normalizing method, where we made subtracted the measurements of the involved side from those of the uninvolved side, and divided this by the torque of the normal side to calculate
Management of spasticity in stroke patients
289 (2002), was not as common as weakness, their effect of spasticity on disability and performance of stroke patients should not be ignored. Spasticity, apart from its negative effects on patients performance, could give rise to muscle contracture (Botte et al., 1988; Harburn and Potter, 1993).
Clinical implications
Figure 5 Frequency and dispersion of Modified Ashworth Scale scores of knee extensor muscle depending on involved side (X axis is spastic muscle and Y axis is subject population).
normalized values, the presence of negative values indicate that in these patients the torque of the involved side was higher than the non-involved side. The relative weakness of the uninvolved side in some stroke patients is consistent with the results of Harris et al. (2001) that concluded weakness develops in the noninvolved side’s quadriceps muscle in stroke patients. Harris and colleagues evaluated the patients in the first week after stroke, while we studied patients at least three months after the stroke event. One possible explanation for this is that some patients may have exerted more effort with their affected side during the isokinetic strength test to show that it has enough strength. However, with comparable results in both studies it seems reasonable to assume that in these patients more attention should be given to the non-involved side. Having a significant direct relationship between spasticity severity and strength that normalized, based on the subtraction method, indicates a negative correlation between the degree of spasticity and strength, and in fact represents the weakness of muscles with more spastic tone in comparison with other muscles. Therefore, in treatment we should place more emphasis on muscles with severe spasticity. However, due to the non-experimental nature of this study, it is not possible to conclude this result directly from this research. A negative significant relationship between degree of spasticity and muscle strength in the lower extremities indicates that spasticity has a negative impact on muscle strength. Therefore, patients with severe spasticity may have weaker muscles, and treatment methods in these stroke patients tend to focus on motor retraining programs. It is not possible to ignore the significant negative effects of spasticity on the function of stroke patients. Probably it seems that spasticity, as an abnormal tone, blocks the development of voluntary muscle tone and obstructs the contractile capacity of the voluntary contraction in muscle. Leathley et al. (2004) demonstrated that if the Barthel index score 7 days after stroke is low, or early muscle weakness is high, we can expect more chance of severe spasticity later. Occurrences of severe spasticity with severe muscle weakness typically presents the possibility that spasticity and strength compete with each other in taking control of muscle contractile capacity. Although the prevalence of spasticity, about 38% as reported by Watkins et al.
The results of this study indicate that, in spastic stroke patients, spasticity management techniques could be used before the application of strengthening techniques. This points to a combination of these two approaches being more useful than the individual application of these treatment methods. As spasticity management may help muscle strength development in its primary stages, it is recommended that the combined treatment procedure should be used in treatment of spastic stroke patients.
Limitations of the study In patients with severe muscle weakness or severe spasticity, it was not possible to test isokinetic muscle strength. So, patients with weak muscles or severe spasticity (measuring 3 or more on the modified Ashworth Scale) were excluded from this study. This has been an observational study, which at most gives us the relationship between the studied variables. Therefore in this study we cannot form conclusions about the causes of changes or relationships. Further studies are required to address these causes.
Suggestions for future research We suggest that research could be conducted to measure the effect of spasticity decrease on spastic muscle strength. And the effect of inhibitory procedures such as reflex inhibitory patterns (RIP) and stretching methods on the muscle tone and strength of spastic muscles in stroke patients could be examined.
Conclusion In this study we found a relationship between severity of spasticity and muscle strength that normalized, based on the subtraction method. The results indicate that there is an opposite relationship between the degree of muscle spasticity and isokinetic muscle strength. This finding indicates that spastic muscles are weaker and the focus of treatment should be on spastic muscles.
Acknowledgments The authors thank physiotherapy staffs of Tabassom rehabilitation center, Baharloo, 7th Tir, Loghman, Alghadir and Ziaian hospitals and physiotherapy department of Social Welfare and Rehabilitation Sciences for supporting this research.
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