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Research Reports |
DU Jette, DSc, PT, is Professor and Program Director, Graduate Program in Physical Therapy, Graduate School for Health Studies, Simmons College, Boston, Mass, and Research Program Manager, Department of Rehabilitation Services, Beth Israel Deaconess Medical Center, Boston, Mass.
MD Slavin, PhD, PT, is Associate Professor, Graduate Program in Physical Therapy, Graduate School for Health Studies, Simmons College
PL Andres, PT, was Research Physical Therapist, Neuromuscular Research Unit, New England Medical Center, and Lecturer in Neurology, Tufts Medical School, Boston, Mass, at the time the data for this study were collected. Ms Andres is currently an independent consultant
TL Munsat, MD, is Director, Neuromuscular Research Unit, Department of Neurology, New England Medical Center, and Professor of Neurology, Tufts Medical School
Address all correspondence to Dr Jette at the Graduate Program in Physical Therapy, Graduate School for Health Studies, 300 The Fenway, Simmons College, Boston, MA 02115 (USA) (djette{at}vmsvax.simmons.edu)
Submitted October 14, 1998;
Accepted March 22, 1999
 | Abstract |
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Key Words: Gait • Muscle performance • lower extremity • Neuromuscular disorders • general
| Introduction |
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 TopAbstract Introduction MethodResultsDiscussionConclusionReferences |
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Amyotrophic lateral sclerosis (ALS) is a motor disease that affects motoneurons in the spinal cord and the brain stem, resulting in progressive muscle weakness and loss of function. Although each patient's rate of disease progression is remarkably linear, muscle force is lost at varying rates, dependent on the type of onset (upper limb, lower limb, or bulbar), the muscle group under consideration, the sex of the patient, and the duration of disease.7 The most common temporal pattern is initial limb involvement with subsequent bulbar symptoms.7 Initially, distal muscles are more severely affected than proximal muscles.7 Flexor muscles demonstrate greater weakness than extensor muscles throughout the course of disease.7 Loss of muscle force in individuals with ALS has been shown to be related to loss of function.8
Many researchers3–6,8–20 have explored the relationship between muscle force and walking ability among individuals with myriad characteristics and diseases. Changes in force production have not been shown to cause a specific change in function, but studies provide support for some type of relationship between force and function.3,6,9,12,14–16,18,20 Several problems of interpretation arise, however, from the types of data and analyses used in these studies. We believe one problem results from the fact that impairments in force production have often been measured using units of force or work.4,6,10–12,15,18 The force or work required for walking must vary as a function of an individual's body size. For example, the lower-extremity force that is adequate for walking in a petite 80-year-old woman may not be adequate to allow a large young man to walk. Additionally, the force generated by a relatively small, yet strong, upper-extremity muscle may be interpreted as weakness if measured in a large lower-extremity muscle. The studies that have addressed the problems associated with using units of force have normalized muscle force data by accounting for a subject's weight14,16 or body mass index (BMI).9 There is evidence, however, that sex differences remain after accounting for BMI.9,20 Furthermore, muscle mass is lower in proportion to height in individuals over 60 years of age than it is in younger individuals,21 and this difference will affect the use of BMI to normalize muscle force. Perry et al18 described force as a percentage of normal, citing unpublished data. Absolute force values, however, appear to have been used in their analyses. Damiano and Abel5 calculated force as a percentage of normal and used these calculations in their analyses. Their subjects, however, were children, and their sample consisted of only 16 subjects.
In most studies, walking ability has been quantified in units of energy expenditure,5,16 speed,3,6,9,11–14,17,18,20 or other gait variables.5,6,17,18 Although certain community functions such as crossing the street during a standard light cycle may be affected by gait speed, the ability to walk in other than an urban, outdoor setting may not be affected by speed. For example, Perry et al17 have shown that although gait speed increased for each higher functional level of walking in individuals with hemiplegia, those who were able to walk independently in the community had a much lower gait speed than did individuals without hemiplegia. In addition, although gait speed distinguished among categories of community walkers who needed assistance or not, the walking speeds of those individuals who were able to walk in the community with some assistance were not different from the walking speeds of those who were considered unlimited in household walking. Moreover, although gait variables such as stride length and speed affect gait efficiency, it seems possible that individuals with inefficient gait may be able to function in the community by reducing their energy demand or accepting short-term high energy demands not normally encountered by individuals without functional limitations. Using discriminant analysis, Perry et al17 were not able to show that stride characteristics allowed differentiation of functional walking categories in patients with hemiplegia.
Because it may be difficult to interpret the clinical importance of, for example, a change of 0.016 m/s in gait speed that is predicted to result from a 1-kg change in force,15 use of categories of walking ability may be more conceptually appealing than use of continuous scales of measurement. In some studies examining the relationship of force to walking, walking ability has been categorized by degree of independence or assistance required in the community or at home.10,17 In one study,10 however, the subjects were hospitalized patients, so the classifications were for very-low-level walking abilities, not including community walking. In 2 other studies in which walking ability was classified according to degree of independence, measurements of muscle force were not made.17,22
In recent studies using continuous measures of force and function, the authors have described the relationship as linear.9,12,18 There is growing evidence, however, that the relationship is curvilinear.13–15 Those studies in which a curvilinear relationship13,14 has been described, as well as some studies in which categories of function have been examined,20 support the concept of a threshold for muscle force for functional activities, above which notable improvements in force do not result in improvements in physical function. Identification of force thresholds for various functional activities has important clinical implications. Knowledge of the level of force below which a person might lose, or above which a person might gain, an important physical function could help focus the type and timing of interventions aimed at prevention, improvement, or palliation.
The purpose of our study was to examine the lower-extremity muscle force associated with 3 levels of walking ability in individuals with ALS. We wanted to ascertain the relationship of normalized muscle force (measured as a percentage of the predicted normal value) for dorsiflexion, knee extension and flexion, and hip extension and flexion to the ability to walk independently in the community, in the community with assistance, and in the home only.
| Method |
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Procedure
Muscle force measures.
The force exerted during maximal voluntary isometric contractions for the muscles selected was measured (in kilograms) using an electronic strain gauge tensiometer.*1 The apparatus consisted of an examination table surrounded by an aluminum orthopedic frame. Adjustable clamps with rings attached to the frame. Adjustable length straps were connected to the strain gauge, which, in turn, was attached to the rings clamped on the frame. The limb to be tested was connected to the other end of the strap. Force was transduced electronically by the amount of distortion within the strain gauge, then amplified and recorded. The protocol used in this study has been described as part of the Tufts Quantitative Neuromuscular Examination (TQNE).23 Intrarater reliability (r =.97–.99) and interrater reliability (r =.92–.99) have been established for dorsiflexion, knee flexion, knee extension, hip flexion, and hip extension in patients with ALS using this protocol.23
Lower-extremity muscles were tested by 1 of 4 physical therapists trained in the protocol.23–25 The protocols for testing muscle force were developed as part of the TQNE by a team that included 2 of the authors. Lower-extremity muscle forces were measured bilaterally. Test positions were ordered to allow for patient comfort and standardization. No warm-up was provided. The same test order of positions was used with each subject at each visit: dorsiflexion, knee flexion, knee extension, hip flexion, and hip extension. We used this test order in an effort to minimize fatigue by keeping the total test time at a minimum and avoiding having the subject change positions multiple times. For each movement, 2 maximal isometric contractions, held for 3 to 4 seconds, were performed 5 to 8 seconds apart. Verbal encouragement was provided, with the tester telling the subject to push as hard as possible against the strap secured to the limb segment. The test generating the higher force was used for data analysis.
To test dorsiflexion, each subject was positioned supine with a strap secured around the metatarsals while the tester stabilized the proximal calf. Knee flexion and extension were tested with the subject sitting with the hip and knee at 90 degrees and a strap placed proximal to the lateral malleolus. During knee flexion testing, the tester stabilized the subject over both shoulders. During knee extension testing, the tester stabilized the subject over the distal thigh. To test hip flexion and extension, the subject was positioned supine with the trunk supported on a wedge. To test hip flexion, the subject's thigh was supported on the table at about 20 degrees of flexion, and the strap was placed proximal to the knee; the knee was positioned at 90 degrees, with leg off the end of the table. The tester supported the opposite lower extremity with the hip and knee at 90 degrees. Hip extension was tested in a similar position, with the hip supported at 20 degrees of flexion with a strap proximal to the knee joint. The tester stabilized the subject over the anterior superior iliac spine.
The predicted normal maximal force (in kilograms) for each movement based on each subject's age, sex, height, and weight was derived using a regression equation based on data from a sample of nearly 500 men and women without known muscle disorders who were tested with the procedure we used.25 For each subject, actual force data for each muscle group were then recorded as a percentage of predicted normal maximal force (%PMF).24 An example of the calculation of %PMF is shown in Table 1. The use of %PMF, in our opinion, avoids the problems encountered in using a measure of force, and we believe it allows comparisons among muscle groups and among individuals of different sizes, ages, and sexes. Because the %PMF values for right and left lower extremities were highly correlated (r =.82–.93), the right lower-extremity values were used in all analyses. Additionally, an average of the %PMF for the 5 movements was calculated for each subject.
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Data Analysis
The data we selected for analysis were those from any 2 consecutive visits in which a subject had all muscle force data recorded and changed from one functional category to the next lower functional category. This selection of data resulted in 3 categories of subjects: (1) subjects who changed from being able to walk independently in the community to being able to walk in the community with assistance (n=78), (2) subjects who changed from being able to walk in the community with assistance to being able to walk only at home (n=63), and (3) subjects who changed from being able to walk only at home to being unable to walk (n=25). Because subjects entered and left the unit at various stages of disease and function and because not all muscle groups were always tested, the subjects in each subset varied. All analyses were performed using SPSS, Version 7.5 for Windows.
In order to determine whether the levels of lower-extremity muscle force are associated with levels of walking ability, descriptive statistics were calculated and box plots were constructed for the %PMF values for each muscle group and for the lower-extremity average at the 2 consecutive visits over which functional status declined by one category in each subset of subjects. Paired t tests were used to determine the differences in mean %PMF for each of the muscle groups and the lower-extremity average across the change in walking ability for each subset of subjects.
| Results |
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TopAbstractIntroductionMethodResultsDiscussionConclusionReferences |
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through 3.
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Change From Walking in the Community With Assistance to Walking Only at Home
The mean lower-extremity average %PMF for the 5 movements was 37.52% (SD=15.17%, range=7.31–79.55) during the last visit that subjects were able to walk in the community with assistance. The %PMF ranged from 48.25% (SD=21.40%, range=12.73–118.46) for hip extension to 25.54% (SD=19.70%, range=0.00–69.87) for dorsiflexion. An average of 8 weeks elapsed before the next visit when subjects were able to walk only at home. The mean lower-extremity average %PMF for the 5 movements was 32.18% (SD=13.83%, range=3.54–75.86); %PMF ranged from 42.47% (SD=22.08%, range=3.76–113.00) for hip extension to 21.36% (SD=18.53%, range=0.00–69.87) for dorsiflexion. The mean decline in %PMF for all movements ranged from 4.18% to 6.53%.
Change From Walking Only at Home to Unable to Walk
The mean lower-extremity average %PMF for the 5 movements was 19.12% (SD=9.08%, range=3.54–38.93) during the visit when subjects were last able to walk at home. The mean %PMF ranged from 32.59% (SD=17.23%, range=3.76–62.39) for hip extension to 8.30% (SD=10.60%, range=0.00–33.34) for dorsiflexion. The mean lower-extremity average %PMF for the 5 movements was 13.70% (SD=7.36%, range=0.00–29.60) during the next visit, 10 weeks later, when patients were unable to walk. The mean %PMF ranged from 21.95% (SD=15.99%, range=0.00–65.95) for hip extension to 5.34% (SD=7.65%, range=0.00–25.93) for dorsiflexion. The mean decline in %PMF for all movements ranged from 2.95% to 10.64%.
| Discussion |
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Use of serial data from individuals with ALS, with their inexorable, linear decline in force over time,27,28 provides a unique opportunity for locating specific muscle force thresholds and describing a profile of lower-extremity muscle force at critical points in time vis-à-vis transitions in function. In a previous study using data from this data set, we analyzed the data from all individuals on their third visit to the clinic.19 This cross-sectional analysis demonstrated that increasing levels of %PMF in all muscle groups improved the chances that individuals would be able to walk in the community as opposed to being limited to the home. The approach to analysis, however, did not allow determination of the level of %PMF at which transitions in function might occur.
Previous studies have shown the relationship between force and walking ability in people without deficits in force-generating capacity3,9,11 as well as in individuals with a variety of diagnoses.5,10,11,16–19 In studies in which walking ability was classified in some manner, the evidence suggests that force generation of the lower-extremity muscles is related to higher functional levels of walking. Damiano and Abel5 found that children with cerebral palsy who were independently walking in the community had greater force-generating capacity than those who were limited in their community walking. Bassey et al9 found that individuals who walked with a walker had lower force-generating capacity than those who did not use a walker. Perry et al17 found that voluntary control of knee muscle contraction in the upright position was related to being able to walk in the community as opposed to being able to walk only at home in patients with hemiplegia. Ferrucci et al15 reported that older women who were unable to walk or walked with an aid had less force in the knee extensors and hip flexors than women who were able to walk with no aids.
Most studies that have used continuous scales to measure walking ability have shown, at best, moderate correlations between force and walking ability, depending on the muscle group and variable analyzed.3,9–15,18,20 Other studies4–6 have demonstrated the force-walking relationship by showing improvements in walking ability with programs designed to improve force. In some studies,3,10,18 investigators have used multiple regression analyses to attempt to determine the factors or muscle groups most predictive of walking ability. This is a compelling endeavor; however, as other studies3,13,14 demonstrate, force measurements within a limb are highly correlated. Multi-collinearity, or correlation among independent variables in a regression analysis, reduces the ability to interpret the results of the analysis.
Because no other studies that have identified muscle force levels required for function have measured muscle force in terms of %PMF, it is somewhat difficult to compare our results. Another problem affecting comparisons is that summary scores for lower-extremity force have been used.9,14 Additionally, force thresholds for different functions related to walking have been described. For example, Sonn et al20 have suggested a threshold of 70 N·m for the knee extensors of women for overall independence in instrumental activities of daily living and a threshold of 120 N·m for men. Bassey et al9 suggested a threshold of 1.2 W/kg of body mass for leg extensor force during unassisted walking. Buchner et al14 described a potential threshold of 275 N·m for total lower-extremity force (sum of knee flexion, knee extension, dorsiflexion, and plantar-flexion groups), above which improvements would not result in increases in gait speed. Ferrucci et al15 found that hip flexor force predicted walking speed only when it was below 15 kg. One problem noted in our analyses as well as those of other authors15 is that despite the fact that muscle force differs among walking categories, force measurements show wide variability within categories of ability and overlap across categories (Figs. 1–3). This finding suggests the difficulty of using measures of central tendency to define thresholds.
Examination of the relationship between force and walking ability in individuals with ALS has some inherent limitations. Because ALS is a disease of both the central nervous system and motoneurons and involves bulbar functions as well, the ability to walk is potentially affected by factors such as reflex integrity, balance,10 depression,11 poor motor control,17,22 and endurance.3,16
Tang et al22 have shown that patterns of motor control in the lower limbs of individuals with incomplete spinal cord injury can help predict characteristics of ambulation such as use of assistive devices. They suggested that timing of muscle contractions and the ability to isolate muscle contractions may affect the ability to ambulate. Perry et al17 demonstrated that, in patients with hemiplegia, the ability to isolate voluntary contractions of the muscle groups of the involved knee was associated with being able to walk in the community. Although the effect of central nervous system symptoms on muscle force and walking ability in people with ALS may be a factor, evidence suggests that motoneuron dysfunction is primarily responsible for the weakness.29 Furthermore, even in people with increased reflex activity, greater force is associated with greater gait speed and cadence and gross motor function.5 The relationship between force and walking in people with ALS may also depend on when the relationship is examined, as well as the way in which force is measured. For example, one study of the relationship of knee flexor torque at 180°/s to walking speed in patients with ALS showed high correlations early in the disease process and moderate correlations later.11
An important limitation of this study is the correlational design. This design does not allow any conclusion regarding the effect of loss of force-generating capacity on decline in walking ability. Additionally, the analyses did not control for the myriad additional factors that might have an impact on walking ability in patients with ALS. The design also included many statistical analyses, leading to an increased possibility of erroneously demonstrating differences in muscle force across categories of walking ability. The reader may refer to Table 3 to evaluate the clinical importance of each of the reported differences in muscle force across categories of walking ability. Another limitation of our study was the lack of testing of the reliability of the classification of walking ability. Classification was accomplished, however, by 4 individuals who worked over a period of 5 to 9 years with patients with ALS in the study setting. An additional potential limitation was the standardization of testing order for muscle groups. Although the order was held constant over time, we cannot discount a possible effect of fatigue for the last muscle group. This fact may limit our ability to draw conclusions about the effect of weakness in specific muscles. The order of testing, however, was the same as that used to derive the norms for muscle force25 and the same as that found in the literature on force testing in patients with ALS.23,24,27
Another potential limitation in interpreting the results of our study is that the categories of walking ability, by their nature, included more than the simple function of walking on a level surface. Walking in the community requires negotiating curbs, obstacles, doors, and possibly stairs. Walking at home requires negotiating obstacles such as furniture, thresholds, and carpets and may depend on the distances between essential areas of the home such as bed and bath. Therefore, the categorization of patients used in this study may actually measure both functional limitations and disability. Based on disablement models,2 we might expect less of an association between muscle force and disability than between muscle force and simple walking. This conceptual problem in the classification scheme might explain the wide overlap of muscle force found across walking classifications.
Disablement models suggest that factors such as coping skills, motivation, and necessity, as well as functional capacity, play a role in determining function.2 In addition, it is possible, given that several muscle groups in the lower-extremity function at more than one joint, that relative force in one muscle group may compensate for weakness in another muscle group in performing an activity.18 Severe neck or trunk weakness may also affect a person's ability to ambulate, despite adequate lower-extremity force. Future studies that examine force and function longitudinally and account for variables that affect both force and walking ability are needed to determine whether clear-cut force thresholds can be identified for meaningful physical abilities.
Based on the findings of previous studies and our own study, few definitive conclusions can be drawn with regard to muscle force thresholds for walking ability. In view of the possible intervening factors, it is possible that the difficulties in identifying thresholds cannot be easilyovercome. We believe, however, that because our methods allowed us to define the relationship between force and walking in terms of conceptually understandable measures of function and easily derived and meaningful measurements of force, we have provided data that can be both useful in further conceptualizing research in this area and a practical starting point for clinicians interested in thinking about patients' prognoses and designing suitable interventions.
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| Footnotes |
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This study was approved by the Institutional Review Board of New England Medical Center.
* Interface Inc, 7401 E Buttherus Dr, Scottsdale, AZ 85260. 
SPSS Inc, 444 N Michigan Ave, Chicago, IL 60611.
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