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Research Reports |
CM Kim, PT, MSc, is Research Associate, Rehabilitation Research Laboratory, GF Strong Rehab Centre, Vancouver, British Columbia, Canada
JJ Eng, PT/OT, PhD, is Associate Professor, School of Rehabilitation Sciences, University of British Columbia, T325-2211 Wesbrook Mall, Vancouver, British Columbia, Canada V6T 2B5 (janicee{at}interchange.ubc.ca), and Rehabilitation Research Laboratory, GF Strong Rehab Centre.
Address all correspondence to Dr Eng
Submitted January 22, 2002;
Accepted August 6, 2002
 | Abstract |
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Key Words: Gait • Strength • Stroke
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 TopAbstract Introduction MethodResultsDiscussionConclusionsReferences |
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Although many traditional approaches to stroke rehabilitation have focused on the reduction of abnormal reflex activity and abnormal movement,3 there is growing evidence that muscle weakness, rather than abnormal reflex activity (which is measured by the resistance to passive movement), is a major limiting factor in physical function, particularly for locomotor tasks, following stroke.4–6 Muscle weakness is a common consequence of stroke.7–9 Possible factors contributing to muscle weakness following cerebral lesions include decreased number of motor units,10 disrupted recruitment order of motor units,11 and decreased motor unit firing rates,12 in addition to muscle atrophy following disuse.13 Recent lower-extremity exercise programs that predominantly consisted of exercises designed to enhance force generation through a large range of motion have shown promising effects on gait and stair-climbing locomotor performance.14–16
Identifying the contribution of the force generated by muscle groups to locomotor function after stroke would help to provide a focus in the assessment and treatment programs aimed at improving locomotor tasks. Muscle force generation and locomotor function have been correlated in people with stroke.17–20 Relationships between isometric forces and tasks such as walking ability on level surfaces,17,18 stair-climbing ability,19 and transfer capacity20 have been identified. Bohannon17 found that the isometric torque of paretic hip extensors, knee flexors, ankle dorsiflexors, and ankle plantar flexors (all measured at a 90° angle) were moderately correlated with gait speed on level surfaces (r=.47-.60), whereas hip flexors, hip abductors, and knee extensors were not correlated. In subsequent studies,4,18 however, Bohannon and colleagues found that the isometric torque of paretic knee extensors also was moderately correlated with gait speed (r=.54-.67).
Although the majority of correlational studies of muscle performance and function have evaluated gait ability on level surfaces, Bohannon and Walsh19 also have studied the locomotor task of stair climbing. They found that the isometric torque of all 5 paretic muscle groups that they tested (hip flexors and extensors, knee flexors and extensors, and ankle dorsiflexors) were correlated with a 6-point descriptive stair-climbing score (r=.73-.85). This ordinal scale consisted of 4 points for level of assistance, 1 point for handrail use, and 1 point for pattern (step-through versus step-to).
Isometric forces, however, reflect only forces at one selected point in the range of motion. Other types of force measurements that evaluate forces throughout a range of motion may be more appropriate in establishing relationships with locomotor activities, which require force to be exerted through a large range of motion. Nakamura et al6 reported that isokinetic torque measurements of the paretic knee extensors were more strongly correlated (r=.79-.87) with gait speed than isometric torque measurements (r=.60-.76) in people with stroke.
There are few studies in which the relationship between isokinetic lower-extremity torque and function in people with stroke has been quantified, and in these studies, only a few selected muscle groups have been explored.5,6,21,22 Nadeau et al5 examined the isokinetic torque of paretic hip flexors and ankle plantar flexors and found the hip flexor torque to be highly correlated with gait speed when walking at a self-selected pace (r=.83) and at a maximum pace (r=.88), whereas ankle plantar-flexor torque was only partly associated with maximum pace (r=.41). Three groups6,21,22 examined the relationship between the isokinetic torque of the paretic knee extensors and gait speed and reported correlations (r=.43-.69 for self-selected pace, r=.47-.87 for maximum pace). Lindmark and Hamrin21 also investigated the knee flexor torque and found correlations (r=.43-.72 for self-selected pace, r=.47-.70 for maximum pace). The contribution of the nonparetic limb to function, we believe, has been largely ignored in the past, and only the nonparetic knee extensors have been evaluated, with conflicting results. The isometric torque of nonparetic knee extensors either lacked a correlation with gait speed6 or had low correlations.18
Although these studies contribute to the growing body of evidence supporting the relationship between muscle force and functional abilities, we contend that there is a lack of comprehensive studies relating muscle force measured through a range of motion to function in people with stroke. The purposes of this study were: (1) to quantify the relationship between isokinetic torque of individual lower-limb muscle groups and 2 locomotor tasks important for independent living (ie, gait on level surfaces and stair-climbing speeds) and (2) to determine whether a multiple linear regression model incorporating the torque of the paretic and nonparetic muscle groups could predict gait and stair-climbing speeds in people with stroke. The major flexor and extensor muscles of both lower extremities were selected because of their important role in walking. Eng and Winter23 reported that the flexion and extension forces of the hip, knee, and ankle accounted for 82% of the total work over a stride as opposed to 15% and 3% in the frontal and transverse planes, respectively.
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TopAbstractIntroductionMethodResultsDiscussionConclusionsReferences |
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Demographic data collected from all participants included age, sex, time since the onset of stroke, the paretic side, level of independence in activities of daily living according to the American Heart Association Functional Classification,26 degree of resistance to passive movement in the knee extensors and ankle plantar flexors, and use of assistive devices. The characteristics of the participants are summarized in Table 1. Resistance to passive movement was evaluated by one of the investigators (CMK) passively flexing and extending the limb using the method described by Ashworth.27 Participants were in a supine position, and the resistance was graded on an ordinal scale from 0 to 5 based on the Modified Ashworth Scale.28
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Lower-extremity torque.
The Kin-Com isokinetic dynamometer* was used to measure the torque of the hip flexors and extensors, knee flexors and extensors, and ankle dorsiflexors and plantar flexors bilaterally. The calibration of the instrument was tested prior to the study with known weights and was accurate to within ±1 N. All participants had a practice session 2 to 4 days before the actual testing day to reduce the learning effect, as recommended by Eng et al.29
An angular velocity of 60°/s was used for the isokinetic tests. This angular velocity was selected because it was similar to the peak angular velocity of the hip and ankle joints during the gait of people with stroke (unpublished data collected by the authors on 5 subjects with chronic stroke walking at their self-selected speed). If a participant was not able to produce torque at an angular velocity of 60°/s, an angular velocity of 30°/s was used for that joint for both limbs. Although we chose these angular velocities to mimic those used during functional activities, we acknowledge that during function there is acceleration and deceleration, not movement at a constant velocity, which occurs with an isokinetic dynamometer.
Average torque was determined for each of the 6 muscle groups for the paretic and nonparetic limbs throughout their available range of motion. This torque measurement protocol has been described previously, and the measurements have been shown to be reliable in people with stroke, with intraclass correlation coefficients greater than .85 for average torque values.29 Positioning and stabilization were done as follows:
Gait performance.
For the assessment of gait performance, participants were asked to walk at their 'most comfortable speed' (ie, self-selected pace) using their usual assistive device for a distance of 8 m 5 times, and then 'as fast as possible' but safely (ie, maximum pace) 5 more times. Participants walked in their own shoes without the use of an orthosis.
Infrared-emitting diodes (IREDs) were attached to the participants' lateral malleoli, and an optoelectronic sensor
was used to track the markers. In this camera setup, the error of locating the coordinates of an IRED in space was 0.9 mm in an anterior-posterior direction and 0.45 mm in an up-down direction. Data were collected at 60 Hz. Gait speed was calculated using the distance covered by the markers and the corresponding elapsed time during each gait cycle. The mean of the 5 trials (in meters per second) was calculated. Gait speed has been recognized as an indicator of gait performance30 and sensitive enough to reflect physiological and functional changes,31 and it has been shown to yield reliable measurements in adults without known pathology.32
Stair-climbing ability.
Participants were asked to climb up four 18-cm steps at their 'most comfortable speed' (ie, self-selected pace) using their usual pattern of foot placement and hand support and then 'safely as fast as possible' (ie, maximum pace). The average time of ascent over 2 trials was calculated for each testing condition (ie, self-selected pace and maximum pace) and converted to stairs per second. This protocol has been described elsewhere32 and has been shown to yield reliable measurements, with reliability coefficients of .90 in 26 adults without known pathology. The reliability of the measurements in people with stroke, however, is not known.
Data Analysis
Descriptive statistics were calculated using SPSS
9.0 for participants' characteristics, gait speed, stair-climbing speed, and torque measures. For the torque measures, average torque values were normalized to body mass. The correlation between each average torque value and the self-selected speed of each task (gait and stair climbing) was established using the Pearson product moment correlation (r) with a significance level of P<.05 (2-tailed). Scatterplots of correlations were visually examined to ensure outliers did not compromise the results of the correlations. The strength of the correlations was described using Munro's33 correlational descriptors (very high=.90-1.00, high=.70-.89, moderate=.50-.69, and low=.26-.49), which provides one method of interpretation for correlation coefficients. Four stepwise multiple linear regression analyses were further used to test whether a model incorporating muscle torque from both lower limbs could predict locomotor performance as measured by (1) self-selected gait speed, (2) maximum gait speed, (3) self-selected stair-climbing speed, and (4) maximum stair-climbing speed. The 12 variables (ie, torque of 2 limbs, 3 joints in flexion and extension) were entered in the model at a significance level of P<.05 and removed from it at P>.10. Normal probability plots for the residuals were checked to ensure that the assumptions of multiple regression were met.
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Relationship Between Torque and Gait Speed on a Level Surface
Although the gait speed on level surfaces of subjects who required the use of an assistive device was only 67% of the speed of those subjects who did not use an assistive device, we found similar correlations between muscle torque and function when subjects were separated into 2 groups (ie, subjects who used an assistive device and subjects who did not use an assistive device). Thus, the data for both groups were pooled for further analyses.
The Pearson product moment correlations (r) between the average torques and gait speeds are presented in Table 4. On the paretic side, the average torques of the hip flexors, knee flexors, and ankle plantar flexors were correlated with gait speed. The correlations (r) were .85 for the ankle plantar flexors, .57 for the hip flexors, and .56 for the knee flexors. On the nonparetic side, only the torques of the knee flexors and ankle plantar flexors were correlated with the gait speeds.
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The variables selected by the multiple regression procedure as predictors of self-selected stair-climbing speed were the paretic ankle plantar flexors, nonparetic knee extensors, and paretic hip extensors, whereas for the maximum stair-climbing speed, only the paretic ankle plantar flexors and the nonparetic knee extensors were retained (Tab. 5).
| Discussion |
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TopAbstractIntroductionMethodResultsDiscussionConclusionsReferences |
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A third limitation is the method in which torque was measured. Not all participants were tested at the same testing speed (eg, for the knee joint, 16 participants were tested at 60°/s and 4 participants were tested at 30°/s), which may have affected the relationship between torque and function. A post hoc subanalysis comparing the regression coefficients36 of the data with and without the data of 6 participants tested at 30°/s for the knee and 2 participants tested at 60°/s for the ankle resulted in no difference between the coefficients, which we believed justified the pooling of the data collected at different speeds. In addition, torque was measured as the average torque generated on a dynamometer without further examination of the strategy (eg, type of activation pattern) used by the subjects to achieve the movements being tested. We believe studies in which electromyographic activity is monitored during testing may be of benefit in understanding the cause of the reduced force output. Likewise, we contend that the assessment of locomotor performance was limited to speed measures without analyzing the strategies used.
Stepwise multiple regression analyses were used to identify the paretic ankle plantar-flexor torque as the single most important variable in predicting gait speed and alone explained 67% to 72% of the variance in gait speeds on level surfaces. For stair-climbing speeds, the torque of the paretic ankle plantar flexors explained 50% to 54% of the variance. Up to 71% of the variance in self-selected stair-climbing speeds could be explained when the torques of the nonparetic knee extensors and paretic hip extensors were added to the model. Similarly, up to 66% of the variance in maximum stair-climbing speeds could be explained when the torques of the nonparetic knee extensors were added to the model. We consider these findings important because a number of factors (eg, balance, coordination, sensation, postural control), in addition to muscle force, may influence the performance of these locomotor tasks.
On the paretic side, the torques obtained for the same 3 muscle groups (hip flexors, knee flexors, and ankle plantar flexors) were found to relate to gait on level surfaces and stair-climbing speed. We did not expect this finding because of the different requirements of these 2 locomotor tasks. In people without strokes or other pathologies, the plantar flexors and hip flexors generate the largest power bursts (ie, largest amount of energy generated to move the body forward) during the entire gait cycle on level surfaces,23 whereas the plantar flexors and knee extensors generate the largest power bursts during stair climbing.37
Thus, the importance of the weakness in the plantar flexors (as identified by the regression analysis and the high correlation coefficient) and hip flexors (as reflected by the moderate correlation coefficient) during gait on level surfaces is logical in view of the power burst that plantar flexors generate during 'push-off' and the torques the hip flexors generate to pull the swinging limb forward.23 The isokinetic torques of the paretic hip flexors and plantar flexors have been previously identified as important factors in determining gait speed.5,38
The correlation between the paretic knee flexor torque and gait performance on level surfaces was surprising to us. The knee flexors' primary function in gait is normally to absorb energy from the swinging limb in late swing.23 The role of the knee flexors during gait in people with hemiparesis, however, may be different from that seen in the gait of people without pathology. Our participants may have needed to flex their knee during propulsion in preparation for swing to compensate for the lack of hip flexion and plantar-flexor push-off, which normally would result in a passive collapse of the knee.39,40 Future investigations on the role of knee flexors in the gait of people with stroke are needed to confirm these hypotheses.
Contrary to the findings of other researchers,6,21,22 the torque of the paretic knees was not associated with gait speed on level surfaces. These contrasting findings may be due to the relatively lower level of function of our subjects. The mean maximum gait speed of our subjects was only 0.69 m/s as compared with the 0.9 to 1.26 m/s documented in other studies.6,21,22 Our findings suggest that weakness in the paretic knee extensors is less limiting than that in other muscle groups during the gait of people with stroke.
The correlations, although low to moderate, of the nonparetic knee flexor and plantar-flexor torques with self-selected gait speed, coupled with reports of bilateral weakness in individuals with stroke,41,42 suggest that torque measurements of the supposedly 'unaffected' limb (as the nonparetic limb is sometimes called) should be included in evaluations.
Ours was the first study in which there was quantification of the relationship between lower-extremity isokinetic torque and the locomotor task of stair climbing in individuals with stroke. Generally, the torque of the paretic limb showed higher correlations with stair-climbing speed than the torque of the nonparetic limb. This finding suggested to us that the weakness in the paretic limb is a more important limiting variable than that of the nonparetic limb during stair climbing.
On the paretic side, the correlations (ranging from low to high) between stair-climbing speed and the torque of hip flexors, knee flexors, and ankle plantar flexors, in addition to the selection of ankle plantar-flexor torque as the best predictor by the regression procedure, can be explained by some of the biomechanical requirements of the stair-climbing task. When ascending stairs, ankle plantar flexors generate power during the latter part of stance to elevate the body.37 The hip and knee flexors concentrically flex the limb during swing in preparation for foot placement on the following step.37 Interestingly, although hip and knee extensors play important roles during the early to mid-stance phases of stair ascent in people without known pathology,37 these variables were not associated with stair ascent in our participants. Because all except one of the participants used the handrail to ascend the stairs, the lifting action of the hip and knee flexors may have been more important than the pushing action of the extensors on the paretic limb in increasing the speed of stair ascent. The arm pulling on the handrail possibly compensated for the lack of hip and knee extensor torque.
Because correlational studies do not infer causation, further research is needed to evaluate whether changing the torque of muscle groups tested in our study would lead to better locomotor performance. Moreover, following stroke, several factors (eg, muscle atrophy, abnormal activation patterns) may contribute to the inability to generate force and, in turn, affect gait performance. The cause of reduced force output needs to be explored in order to determine the type of intervention that may lead to improved torque and function.
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| Footnotes |
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This study was approved by the University of British Columbia Research Ethics Board and the GF Strong Rehab Centre Research Advisory and Review Committee.
* Chattanooga Group Inc, 4717 Adams Rd, Hixson, TN 37343. 
Northern Digital, 103 Randall Dr, Waterloo, Ontario, Canada N2V 1C5.
SPSS Inc, 233 S Wacker Dr, Chicago, IL 60606.
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