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References Pathophysiology
Bohannon, R. W. (1983). Results of Resistance Exercise on a
Patient with Amyotrophic Lateral Sclerosis. Phys. Ther, 63(6),
965–968. doi: 10.1093/ptj/63.6.965
Goodman, C. C., & Marshall, C. (2017). Pathology for the
physical therapist assistant. Philadelphia: Saunders.
Jette, D. U., Slavin, M. D., Andres, P. L., & Munsat, T. L.
(1999). The Relationship of Lower-Limb Muscle Force to
Walking Ability in Patients with Amyotrophic Lateral
Sclerosis. Phys Ther, 79(7), 672–681. doi: 10.1093/ptj/79.7.672
Martin, S., & Kessler, M. (2016). Neurologic interventions for
physical therapy. St. Louis: Elsevier Saunders.
Bello-Haas, V. D., Kloos, A. D., & Mitsumoto, H. (1998).
Physical Therapy for a Patient Through Six Stages of
Amyotrophic Lateral Sclerosis. Phys. Ther, 78(12), 1312–1324.
doi: 10.1093/ptj/78.12.1312
The Relationship of Lower-Limb
Muscle Force to Walking Ability in
Patients With Amyotrophic
Lateral Sclerosis
Background and Purpose. The purpose of this study was to
determine
the level of muscle force associated with ability to walk in the
community without assistance, in the community with
assistance, or at
home only in individuals with amyotrophic lateral sclerosis
(ALS).
Subjects and Methods. Percentage of predicted maximal muscle
force
(%PMF) of lower-extremity muscles was determined, and
walking
ability was categorized in 118 patients with ALS during
periodic visits to
the Neuromuscular Research Unit. Data were derived from
consecu-
tive visits in which subjects demonstrated declines in walking
ability.
Means for %PMF of each muscle group and a limb average were
calculated at each consecutive visit. Results. The mean lower-
extremity
average %PMF was: (1) 54.01% (SD512.76%) for subjects who
walked
independently in the community and 50.19% (SD514.38%)
during
the next visit when these same subjects required assistance in
the
community (difference53.82%, 95% confidence interval [CI]5
2.4525.19);(2) 37.52% (SD515.17%) during the last visit that
subjects
walked with assistance in the community and 32.18%
(SD513.83%)
during the next visit when they walked only at home (differ-
ence55.33%, 95% CI53.61–7.06); and (3) 19.12% (SD59.08%)
dur-
ing the visit when subjects were last able to ambulate at home
versus
13.70% (SD57.36%) when they became unable to walk (differ-
ence55.42%, 95% CI52.9727.96). Conclusion and Discussion.
The
findings suggest there are required levels of lower-extremity
muscle
force for various categories of walking ability. Variations in
forces
within and between categories of walking ability, however,
indicate the
complexity of this relationship. [Jette DU, Slavin MD, Andres
PL,
Munsat TL. The relationship of lower-limb muscle force to
walking
ability in patients with amyotrophic lateral sclerosis. Phys Ther.
1999;79:672– 681.]
Key Words: Gait; Muscle performance, lower extremity;
Neuromuscular disorders, general.
672 Physical Therapy . Volume 79 . Number 7 . July 1999
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Diane U Jette
Mary D Slavin
Patricia L Andres
Theodore L Munsat
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T
he disablement models1,2 suggest a relationship
between impairments such as diminished mus-
cle force and functional limitations such as
difficulty walking. These relationships have
been explored by researchers studying whether interven-
tions directed at ameliorating impairments produce
improvements in function or prevent functional limita-
tion.3– 6 We believe that understanding the nature of
such relationships is critical because many, if not most,
treatments provided by physical therapists are based on
the assumption that altering impairment leads to
improved function.
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 individ-
uals 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 func-
tion.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
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. 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)
([email protected]).
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.
Concept and research design were provided by Jette, Slavin,
Andres, and Munsat; writing, by Jette and Slavin; data
collection, by Andres; data
analysis, by Jette; fund procurement, by Munsat; subjects, by
Andres and Munsat; facilities and equipment, by Andres;
institutional liaisons, by
Munsat; and consultation (including review of manuscript prior
to submission), by Slavin, Andres, and Munsat.
This study was approved by the Institutional Review Board of
New England Medical Center.
This article was submitted October 14, 1998, and accepted
March 22, 1999.
Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al
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large young man to walk. Additionally, the force gener-
ated 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 hemiple-
gia, 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 unlim-
ited in household walking. Moreover, although gait
variables such as stride length and speed affect gait
efficiency, it seems possible that individuals with ineffi-
cient 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 dis-
criminant analysis, Perry et al17 were not able to show
that stride characteristics allowed differentiation of func-
tional 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 abil-
ities, 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 relation-
ship 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 thresh-
old 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 func-
tion could help focus the type and timing of interven-
tions 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 exten-
sion and flexion to the ability to walk independently in
the community, in the community with assistance, and in
the home only.
Method
Subjects
Data from 118 patients were retrospectively analyzed for
our study. Data were drawn from a data set containing
information from 662 patients with ALS referred to the
New England Medical Center Neuromuscular Research
Unit from 1979 to 1995. Patients were referred to the
laboratory to confirm the diagnosis of ALS, monitor
clinical disease progression, or participate in clinical
trials. All subjects signed informed consent forms. Sub-
jects were scheduled for periodic visits and had a median
of 5 visits (minimum51, maximum555). The mean age
of the larger sample of subjects at their first visit was
58.38 years (SD512.21, range522.65– 85.95); 58% were
men and 42% were women.
Procedure
Muscle force measures. The force exerted during max-
imal voluntary isometric contractions for the muscles
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selected was measured (in kilograms) using an elec-
tronic strain gauge tensiometer.*1 The apparatus con-
sisted of an examination table surrounded by an alumi-
num 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 Neuromuscu-
lar Examination (TQNE).23 Intrarater reliability
(r 5.97–.99) and interrater reliability (r 5.92–.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 sup-
ported 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 5.82–
.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.
Walking ability classification. Hoffer et al26 described
functional ambulation categories for children with myelo-
dysplasia, distinguishing between the ability to ambulate
in the community and at home. We modified these
criteria for our study. Each subject’s walking ability was
classified, through patient interview and observation,
into 1 of 4 categories by 1 of the 4 physical therapists
trained in the protocol. The categories were: unable to
walk (the patient cannot ambulate even with assistance),
walking only at home (the patient can ambulate in the
home with or without assistance or assistive devices but
cannot walk in the community), walking in the commu-
nity with assistance (the patient can ambulate in the
community but requires the assistance of a device or
another person), or independent walking in the com-
munity (the patient can walk independently in the
community without assistive devices). The validity of the
scale has been supported by work by Perry et al.17 The*
Interface Inc, 7401 E Buttherus Dr, Scottsdale, AZ 85260.
Table 1.
Sample Calculation of Percentage of Predicted Normal Maximal
Isometric Force (%PMF)a
Predicted normal right knee extension for a 50-year-
old man who weighs 180 lb and is 72 in tall:
Regression equation: Predicted Normal Isometric Force5
(Sex 3 13.95) 2 (Age 3 0.38) 1 (Weight 3 0.14) 1
(Height 3 0.08) 1 24.60
5 (13.95) 2 (19) 1 (25.2) 1 (5.76) 1 24.60
5 50.51 kg
Subject’s actual right knee extension force is 31 kg,
%PMF 5 (31/50.51) 3 100 5 61%
a 1 lb50.4536 kg, 1 in52.54 cm.
Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al
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reliability, however, has not been tested. Because the
functional status of patients with ALS declines at varying
rates and the time between visits varied, subjects often
remained in the same walking category for several visits.
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 cate-
gory 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 (n578), (2) subjects who changed from
being able to walk in the community with assistance
to being able to walk only at home (n563), and
(3) subjects who changed from being able to walk only at
home to being unable to walk (n525). 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
Ages and sexes for each subset of subjects are shown in
Table 2. For all subsets of subjects, the mean %PMF at
each functional level was greatest at the hip and lowest at
the ankle. In each subset of subjects, there was a
decrease in %PMF in all muscle groups from the visit
during which the walking function was higher to the visit
during which the walking function was lower. Data are
displayed in Table 3 and in Figures 1 through 3.
Change From Walking Independently in the Community
to Walking in the Community With Assistance
The mean lower-extremity average %PMF for the 5
movements was 54.01% (SD512.76%, range518.77–
84.23) during the last visit when subjects were able to
walk independently in the community. Measurements
of %PMF ranged from 66.45% (SD521.59%,
range530.20 –136.21) for hip extension to 40.18%
(SD522.30%, range50.00 –92.90) for dorsiflexion. Dur-
ing the next visit when subjects required assistance in the
community, an average of 7 weeks had elapsed. The
mean lower-extremity average %PMF was 50.19%
(SD514.38%, range516.05– 89.22), ranging from
62.08% (SD520.35%, range520.37–128.48) for hip
extension to 36.76% (SD522.53%, range50.00 – 86.90)
for dorsiflexion. The mean decline in %PMF of all
muscle groups ranged from 2.76% to 4.37%.
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% (SD515.17%, range57.31–
79.55) during the last visit that subjects were able to walk
in the community with assistance. The %PMF ranged
from 48.25% (SD521.40%, range512.73–118.46) for
hip extension to 25.54% (SD519.70%, range50.00 –
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% (SD513.83%,
range53.54 –75.86); %PMF ranged from 42.47%
(SD522.08%, range53.76 –113.00) for hip extension to
21.36% (SD518.53%, range50.00 – 69.87) for dorsiflex-
ion. 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% (SD59.08%, range53.54 –
38.93) during the visit when subjects were last able to
walk at home. The mean %PMF ranged from 32.59%
(SD517.23%, range53.76 – 62.39) for hip extension to
8.30% (SD510.60%, range50.00 –33.34) for dorsiflex-
ion. The mean lower-extremity average %PMF for the 5
movements was 13.70% (SD57.36%, range50.00 –
29.60) during the next visit, 10 weeks later, when
patients were unable to walk. The mean %PMF ranged
from 21.95% (SD515.99%, range50.00 – 65.95) for hip
extension to 5.34% (SD57.65%, range50.00 –25.93) for
dorsiflexion. The mean decline in %PMF for all move-
ments ranged from 2.95% to 10.64%.
Discussion
The decline in walking ability observed in our subjects
appears to have been precipitated by relatively small
changes in muscle force, suggesting the possibility of
force thresholds below which walking cannot be main-
tained. The data suggest that, on average, the transition
from independent walking to walking in the community
with assistance occurs when the average lower-extremity
%PMF drops below approximately 54%. The transition
from walking in the community with assistance to being
able to walk only at home occurs when the average
lower-extremity %PMF drops below approximately 37%.
With an average lower-extremity %PMF of less than
† SPSS Inc, 444 N Michigan Ave, Chicago, IL 60611.
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approximately 19%, individuals are no longer able to
walk in the home. Consistent with the pattern and
progression of ALS described in the literature,7 we
found greater losses of muscle force in the distal mus-
culature as compared with the proximal musculature at
every functional walking category.
Use of serial data from individuals with ALS, with their
inexorable, linear decline in force over time,27,28 pro-
vides 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
Table 2.
Sample Demographics
Age (y) Sex (%)
X SD Range Male Female
Independent community walking to 52.4 11.1 26.26 –76.22 61
39
assisted community walking (n578) 52.6 11.1 26.35–76.38
Assisted community walking to 53.5 11.1 26.41–76.78 48 52
walking only at home (n563) 53.7 11.0 26.50 –76.93
Walking only at home to 56.4 8.0 38.07–71.19 40 60
unable to walk (n525) 56.6 8.0 38.19 –71.52
Full sample (N5662) 58.38 12.21 22.65– 85.95 58 42
Table 3.
Percentage of Predicted Muscle Force at Transitions in Walking
Ability
Dorsiflexion Knee Flexion
Knee
Extension Hip Flexion Hip Extension
Limb
Average
Independent community walking
X 40.18 52.42 52.37 63.88 66.45 54.01
SD 22.30 18.39 19.79 17.01 21.59 12.76
Range 0.00 –92.90 18.10 –105.20 9.83–113.18 18.02–116.96
30.20 –136.21 18.77– 84.23
Assisted community walking
X 36.76 48.95 48.31 61.12 62.08 50.19
SD 22.53 19.39 45.11 18.92 20.35 14.38
Range 0.00 – 86.90 13.47–102.02 7.50 –108.80 19.44 –110.53
20.37–128.48 16.05– 89.22
Difference
X 3.42 3.48 4.07 2.76 4.37 3.82
CIa 0.58 – 6.26 2.65– 6.09 2.19 –5.94 0.09 –5.61 1.99 – 6.75
2.45–5.19
Assisted community walking
X 25.54 33.65 38.69 46.84 48.25 37.52
SD 19.70 19.39 21.37 20.91 21.40 15.17
Range 0.00 –78.51 1.77– 87.97 2.04 – 86.23 6.08 –108.41
12.73–118.46 7.31–79.55
Walking only at home
X 21.36 27.12 33.56 42.32 42.47 32.18
SD 18.53 16.66 19.26 19.37 22.08 13.83
Range 0.00 – 69.87 1.18 –79.18 3.07–71.98 6.29 –96.38 3.76 –
113.00 3.54 –75.86
Difference
X 4.18 6.53 5.13 4.52 5.77 5.33
CI 1.38 – 6.99 4.15– 8.91 3.02–7.24 1.78 –7.27 2.79 – 8.75
3.61–7.06
Walking only at home
X 8.30 11.31 20.86 26.18 32.59 19.12
SD 10.60 8.48 11.18 17.39 17.23 9.08
Range 0.00 –33.34 0.00 –27.81 2.57– 40.38 0.00 – 85.01 3.76 –
62.39 3.54 –38.93
Unable to walk
X 5.34 7.51 15.64 20.56 21.95 13.70
SD 7.65 6.21 9.74 13.92 15.99 7.36
Range 0.00 –25.93 0.00 –20.95 0.00 –34.99 0.00 – 61.66 0.00 –
65.95 0.00 –29.60
Difference
X 2.95 3.80 5.22 5.62 10.64 5.42
CI 0.76 –5.14 1.60 – 6.00 3.12–7.32 1.77–9.47 4.48 –16.81
2.97–7.86
a CI5confidence interval.
Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al
. 677
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from this data set, we analyzed the data from all individ-
uals 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 evi-
dence 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. Fer-
rucci et al15 reported that older women
who were unable to walk or walked with
an aid had less force in the knee exten-
sors 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 stud-
ies4 – 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 walk-
ing ability. This is a compelling endeav-
or; however, as other studies3,13,14 dem-
onstrate, force measurements within a
limb are highly correlated. Multi-
collinearity, or correlation among inde-
pendent variables in a regression anal-
ysis, 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 com-
parisons 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 Nzm for the knee extensors of women for
overall independence in instrumental activities of daily
living and a threshold of 120 Nzm 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 Nzm 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 sug-
gests the difficulty of using measures of central tendency
to define thresholds.
Figure 1.
Distributions of percentage of predicted muscle force (%PMF)
of lower-extremity movements
according to walking ability in patients during the transition
from walking independently in the
community to walking with assistance in the community (n578).
The dark line in the center of
each box represents the median. The upper and lower bounds of
each box represent the 75th
and 25th percentiles, respectively. The lines extending from the
boxes represent the highest and
the lowest values that are not outliers. The circles represent
values more that 1.5 box lengths
from the highest or lowest values (outliers).
678 . Jette et al Physical Therapy . Volume 79 . Number 7 . July
1999
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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 func-
tions as well, the ability to walk is poten-
tially 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 volun-
tary 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 Further-
more, 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 dem-
onstrating 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 categoriza-
tion 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 associ-
ation between muscle force and disability than between
Figure 2.
Distributions of percentage of predicted muscle force (%PMF)
of lower-extremity movements
according to walking ability in patients during the transition
from walking with assistance in the
community to walking only at home (n563). The dark line in the
center of each box represents
the median. The upper and lower bounds of each box represent
the 75th and 25th percentiles,
respectively. The lines extending from the boxes represent the
highest and the lowest values that
are not outliers. The circles represent values more that 1.5 box
lengths from the highest or lowest
values (outliers).
Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al
. 679
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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 addi-
tion, 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.
Conclusion
This study provides a profile of lower-
extremity muscle force at critical tran-
sitions in walking ability in patients with
ALS. For each of the lower-extremity
movements tested, there was a decrease
in %PMF from the subject’s visit during
which the walking function was at a
higher level to the next visit during
which the function was lower. The find-
ings of our study provide support for a
relationship between impairment and
functional limitation and suggest possi-
ble thresholds for lower-extremity mus-
cle force required for various func-
tional levels of walking. Wide variations
in muscle forces within and between categories of walk-
ing ability, however, suggest the difficulty of identifying
force thresholds related to physical functions.
References
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Distributions of percentage of predicted muscle force (%PMF)
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from walking only at home to being
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represents the median. The upper
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percentiles, respectively. The lines
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circles represent values more that 1.5 box lengths from the
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Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al
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Miguel JuncoReferences PathophysiologyBohannon, R. W. (1983). .docx

  • 1. Miguel Junco References Pathophysiology Bohannon, R. W. (1983). Results of Resistance Exercise on a Patient with Amyotrophic Lateral Sclerosis. Phys. Ther, 63(6), 965–968. doi: 10.1093/ptj/63.6.965 Goodman, C. C., & Marshall, C. (2017). Pathology for the physical therapist assistant. Philadelphia: Saunders. Jette, D. U., Slavin, M. D., Andres, P. L., & Munsat, T. L. (1999). The Relationship of Lower-Limb Muscle Force to Walking Ability in Patients with Amyotrophic Lateral Sclerosis. Phys Ther, 79(7), 672–681. doi: 10.1093/ptj/79.7.672 Martin, S., & Kessler, M. (2016). Neurologic interventions for physical therapy. St. Louis: Elsevier Saunders. Bello-Haas, V. D., Kloos, A. D., & Mitsumoto, H. (1998). Physical Therapy for a Patient Through Six Stages of Amyotrophic Lateral Sclerosis. Phys. Ther, 78(12), 1312–1324. doi: 10.1093/ptj/78.12.1312 The Relationship of Lower-Limb Muscle Force to Walking Ability in Patients With Amyotrophic Lateral Sclerosis Background and Purpose. The purpose of this study was to determine the level of muscle force associated with ability to walk in the community without assistance, in the community with assistance, or at home only in individuals with amyotrophic lateral sclerosis (ALS).
  • 2. Subjects and Methods. Percentage of predicted maximal muscle force (%PMF) of lower-extremity muscles was determined, and walking ability was categorized in 118 patients with ALS during periodic visits to the Neuromuscular Research Unit. Data were derived from consecu- tive visits in which subjects demonstrated declines in walking ability. Means for %PMF of each muscle group and a limb average were calculated at each consecutive visit. Results. The mean lower- extremity average %PMF was: (1) 54.01% (SD512.76%) for subjects who walked independently in the community and 50.19% (SD514.38%) during the next visit when these same subjects required assistance in the community (difference53.82%, 95% confidence interval [CI]5 2.4525.19);(2) 37.52% (SD515.17%) during the last visit that subjects walked with assistance in the community and 32.18% (SD513.83%) during the next visit when they walked only at home (differ- ence55.33%, 95% CI53.61–7.06); and (3) 19.12% (SD59.08%) dur- ing the visit when subjects were last able to ambulate at home versus 13.70% (SD57.36%) when they became unable to walk (differ- ence55.42%, 95% CI52.9727.96). Conclusion and Discussion. The findings suggest there are required levels of lower-extremity muscle force for various categories of walking ability. Variations in forces
  • 3. within and between categories of walking ability, however, indicate the complexity of this relationship. [Jette DU, Slavin MD, Andres PL, Munsat TL. The relationship of lower-limb muscle force to walking ability in patients with amyotrophic lateral sclerosis. Phys Ther. 1999;79:672– 681.] Key Words: Gait; Muscle performance, lower extremity; Neuromuscular disorders, general. 672 Physical Therapy . Volume 79 . Number 7 . July 1999 Re se ar ch Re po rt Diane U Jette Mary D Slavin Patricia L Andres Theodore L Munsat v IIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIII IIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIII IIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIIII IIIIIIIIIIII
  • 5. ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 T he disablement models1,2 suggest a relationship between impairments such as diminished mus- cle force and functional limitations such as difficulty walking. These relationships have been explored by researchers studying whether interven- tions directed at ameliorating impairments produce improvements in function or prevent functional limita- tion.3– 6 We believe that understanding the nature of such relationships is critical because many, if not most, treatments provided by physical therapists are based on the assumption that altering impairment leads to improved function. 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
  • 6. 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 individ- uals 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 func- tion.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 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. Address all correspondence to Dr Jette at the Graduate
  • 7. Program in Physical Therapy, Graduate School for Health Studies, 300 The Fenway, Simmons College, Boston, MA 02115 (USA) ([email protected]). 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. Concept and research design were provided by Jette, Slavin, Andres, and Munsat; writing, by Jette and Slavin; data collection, by Andres; data analysis, by Jette; fund procurement, by Munsat; subjects, by Andres and Munsat; facilities and equipment, by Andres; institutional liaisons, by Munsat; and consultation (including review of manuscript prior to submission), by Slavin, Andres, and Munsat. This study was approved by the Institutional Review Board of New England Medical Center. This article was submitted October 14, 1998, and accepted March 22, 1999.
  • 8. Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al . 673 III III III III III III III III III III III III III III III III III III III III III III
  • 10. /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 large young man to walk. Additionally, the force gener- ated 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
  • 11. 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 hemiple- gia, 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 unlim- ited in household walking. Moreover, although gait variables such as stride length and speed affect gait efficiency, it seems possible that individuals with ineffi- cient 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 dis- criminant analysis, Perry et al17 were not able to show that stride characteristics allowed differentiation of func- tional 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
  • 12. 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 abil- ities, 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 relation- ship 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 thresh- old 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 func- tion could help focus the type and timing of interven- tions 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 exten- sion and flexion to the ability to walk independently in the community, in the community with assistance, and in the home only. Method
  • 13. Subjects Data from 118 patients were retrospectively analyzed for our study. Data were drawn from a data set containing information from 662 patients with ALS referred to the New England Medical Center Neuromuscular Research Unit from 1979 to 1995. Patients were referred to the laboratory to confirm the diagnosis of ALS, monitor clinical disease progression, or participate in clinical trials. All subjects signed informed consent forms. Sub- jects were scheduled for periodic visits and had a median of 5 visits (minimum51, maximum555). The mean age of the larger sample of subjects at their first visit was 58.38 years (SD512.21, range522.65– 85.95); 58% were men and 42% were women. Procedure Muscle force measures. The force exerted during max- imal voluntary isometric contractions for the muscles 674 . Jette et al Physical Therapy . Volume 79 . Number 7 . July 1999 D ow nloaded from https://academ ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA
  • 14. M em ber A ccess user on 18 M arch 2020 selected was measured (in kilograms) using an elec- tronic strain gauge tensiometer.*1 The apparatus con- sisted of an examination table surrounded by an alumi- num 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 Neuromuscu- lar Examination (TQNE).23 Intrarater reliability (r 5.97–.99) and interrater reliability (r 5.92–.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
  • 15. 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 sup- ported 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,
  • 16. 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 5.82– .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. Walking ability classification. Hoffer et al26 described functional ambulation categories for children with myelo- dysplasia, distinguishing between the ability to ambulate in the community and at home. We modified these criteria for our study. Each subject’s walking ability was classified, through patient interview and observation, into 1 of 4 categories by 1 of the 4 physical therapists trained in the protocol. The categories were: unable to walk (the patient cannot ambulate even with assistance), walking only at home (the patient can ambulate in the home with or without assistance or assistive devices but cannot walk in the community), walking in the commu- nity with assistance (the patient can ambulate in the community but requires the assistance of a device or another person), or independent walking in the com- munity (the patient can walk independently in the community without assistive devices). The validity of the scale has been supported by work by Perry et al.17 The* Interface Inc, 7401 E Buttherus Dr, Scottsdale, AZ 85260.
  • 17. Table 1. Sample Calculation of Percentage of Predicted Normal Maximal Isometric Force (%PMF)a Predicted normal right knee extension for a 50-year- old man who weighs 180 lb and is 72 in tall: Regression equation: Predicted Normal Isometric Force5 (Sex 3 13.95) 2 (Age 3 0.38) 1 (Weight 3 0.14) 1 (Height 3 0.08) 1 24.60 5 (13.95) 2 (19) 1 (25.2) 1 (5.76) 1 24.60 5 50.51 kg Subject’s actual right knee extension force is 31 kg, %PMF 5 (31/50.51) 3 100 5 61% a 1 lb50.4536 kg, 1 in52.54 cm. Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al . 675 III III III III III III III III I
  • 18. D ow nloaded from https://academ ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 reliability, however, has not been tested. Because the functional status of patients with ALS declines at varying rates and the time between visits varied, subjects often remained in the same walking category for several visits. 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 cate- gory 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 (n578), (2) subjects who changed from
  • 19. being able to walk in the community with assistance to being able to walk only at home (n563), and (3) subjects who changed from being able to walk only at home to being unable to walk (n525). 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 Ages and sexes for each subset of subjects are shown in Table 2. For all subsets of subjects, the mean %PMF at each functional level was greatest at the hip and lowest at the ankle. In each subset of subjects, there was a decrease in %PMF in all muscle groups from the visit during which the walking function was higher to the visit during which the walking function was lower. Data are displayed in Table 3 and in Figures 1 through 3. Change From Walking Independently in the Community to Walking in the Community With Assistance The mean lower-extremity average %PMF for the 5 movements was 54.01% (SD512.76%, range518.77– 84.23) during the last visit when subjects were able to
  • 20. walk independently in the community. Measurements of %PMF ranged from 66.45% (SD521.59%, range530.20 –136.21) for hip extension to 40.18% (SD522.30%, range50.00 –92.90) for dorsiflexion. Dur- ing the next visit when subjects required assistance in the community, an average of 7 weeks had elapsed. The mean lower-extremity average %PMF was 50.19% (SD514.38%, range516.05– 89.22), ranging from 62.08% (SD520.35%, range520.37–128.48) for hip extension to 36.76% (SD522.53%, range50.00 – 86.90) for dorsiflexion. The mean decline in %PMF of all muscle groups ranged from 2.76% to 4.37%. 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% (SD515.17%, range57.31– 79.55) during the last visit that subjects were able to walk in the community with assistance. The %PMF ranged from 48.25% (SD521.40%, range512.73–118.46) for hip extension to 25.54% (SD519.70%, range50.00 – 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% (SD513.83%, range53.54 –75.86); %PMF ranged from 42.47% (SD522.08%, range53.76 –113.00) for hip extension to 21.36% (SD518.53%, range50.00 – 69.87) for dorsiflex- ion. 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% (SD59.08%, range53.54 – 38.93) during the visit when subjects were last able to
  • 21. walk at home. The mean %PMF ranged from 32.59% (SD517.23%, range53.76 – 62.39) for hip extension to 8.30% (SD510.60%, range50.00 –33.34) for dorsiflex- ion. The mean lower-extremity average %PMF for the 5 movements was 13.70% (SD57.36%, range50.00 – 29.60) during the next visit, 10 weeks later, when patients were unable to walk. The mean %PMF ranged from 21.95% (SD515.99%, range50.00 – 65.95) for hip extension to 5.34% (SD57.65%, range50.00 –25.93) for dorsiflexion. The mean decline in %PMF for all move- ments ranged from 2.95% to 10.64%. Discussion The decline in walking ability observed in our subjects appears to have been precipitated by relatively small changes in muscle force, suggesting the possibility of force thresholds below which walking cannot be main- tained. The data suggest that, on average, the transition from independent walking to walking in the community with assistance occurs when the average lower-extremity %PMF drops below approximately 54%. The transition from walking in the community with assistance to being able to walk only at home occurs when the average lower-extremity %PMF drops below approximately 37%. With an average lower-extremity %PMF of less than † SPSS Inc, 444 N Michigan Ave, Chicago, IL 60611. 676 . Jette et al Physical Therapy . Volume 79 . Number 7 . July 1999 D ow nloaded from https://academ
  • 22. ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 approximately 19%, individuals are no longer able to walk in the home. Consistent with the pattern and progression of ALS described in the literature,7 we found greater losses of muscle force in the distal mus- culature as compared with the proximal musculature at every functional walking category. Use of serial data from individuals with ALS, with their inexorable, linear decline in force over time,27,28 pro- vides 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 Table 2. Sample Demographics Age (y) Sex (%)
  • 23. X SD Range Male Female Independent community walking to 52.4 11.1 26.26 –76.22 61 39 assisted community walking (n578) 52.6 11.1 26.35–76.38 Assisted community walking to 53.5 11.1 26.41–76.78 48 52 walking only at home (n563) 53.7 11.0 26.50 –76.93 Walking only at home to 56.4 8.0 38.07–71.19 40 60 unable to walk (n525) 56.6 8.0 38.19 –71.52 Full sample (N5662) 58.38 12.21 22.65– 85.95 58 42 Table 3. Percentage of Predicted Muscle Force at Transitions in Walking Ability Dorsiflexion Knee Flexion Knee Extension Hip Flexion Hip Extension Limb Average Independent community walking X 40.18 52.42 52.37 63.88 66.45 54.01 SD 22.30 18.39 19.79 17.01 21.59 12.76 Range 0.00 –92.90 18.10 –105.20 9.83–113.18 18.02–116.96 30.20 –136.21 18.77– 84.23 Assisted community walking X 36.76 48.95 48.31 61.12 62.08 50.19 SD 22.53 19.39 45.11 18.92 20.35 14.38 Range 0.00 – 86.90 13.47–102.02 7.50 –108.80 19.44 –110.53 20.37–128.48 16.05– 89.22
  • 24. Difference X 3.42 3.48 4.07 2.76 4.37 3.82 CIa 0.58 – 6.26 2.65– 6.09 2.19 –5.94 0.09 –5.61 1.99 – 6.75 2.45–5.19 Assisted community walking X 25.54 33.65 38.69 46.84 48.25 37.52 SD 19.70 19.39 21.37 20.91 21.40 15.17 Range 0.00 –78.51 1.77– 87.97 2.04 – 86.23 6.08 –108.41 12.73–118.46 7.31–79.55 Walking only at home X 21.36 27.12 33.56 42.32 42.47 32.18 SD 18.53 16.66 19.26 19.37 22.08 13.83 Range 0.00 – 69.87 1.18 –79.18 3.07–71.98 6.29 –96.38 3.76 – 113.00 3.54 –75.86 Difference X 4.18 6.53 5.13 4.52 5.77 5.33 CI 1.38 – 6.99 4.15– 8.91 3.02–7.24 1.78 –7.27 2.79 – 8.75 3.61–7.06 Walking only at home X 8.30 11.31 20.86 26.18 32.59 19.12 SD 10.60 8.48 11.18 17.39 17.23 9.08 Range 0.00 –33.34 0.00 –27.81 2.57– 40.38 0.00 – 85.01 3.76 – 62.39 3.54 –38.93 Unable to walk X 5.34 7.51 15.64 20.56 21.95 13.70 SD 7.65 6.21 9.74 13.92 15.99 7.36 Range 0.00 –25.93 0.00 –20.95 0.00 –34.99 0.00 – 61.66 0.00 – 65.95 0.00 –29.60 Difference
  • 25. X 2.95 3.80 5.22 5.62 10.64 5.42 CI 0.76 –5.14 1.60 – 6.00 3.12–7.32 1.77–9.47 4.48 –16.81 2.97–7.86 a CI5confidence interval. Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al . 677 III III III III III III III III I D ow nloaded from https://academ ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M
  • 26. em ber A ccess user on 18 M arch 2020 from this data set, we analyzed the data from all individ- uals 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 evi- dence 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
  • 27. home in patients with hemiplegia. Fer- rucci et al15 reported that older women who were unable to walk or walked with an aid had less force in the knee exten- sors 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 stud- ies4 – 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 walk- ing ability. This is a compelling endeav- or; however, as other studies3,13,14 dem- onstrate, force measurements within a limb are highly correlated. Multi- collinearity, or correlation among inde- pendent variables in a regression anal- ysis, 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 com- parisons is that summary scores for lower-extremity force
  • 28. 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 Nzm for the knee extensors of women for overall independence in instrumental activities of daily living and a threshold of 120 Nzm 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 Nzm 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 sug- gests the difficulty of using measures of central tendency to define thresholds. Figure 1. Distributions of percentage of predicted muscle force (%PMF) of lower-extremity movements according to walking ability in patients during the transition from walking independently in the community to walking with assistance in the community (n578). The dark line in the center of each box represents the median. The upper and lower bounds of each box represent the 75th and 25th percentiles, respectively. The lines extending from the boxes represent the highest and the lowest values that are not outliers. The circles represent values more that 1.5 box lengths from the highest or lowest values (outliers).
  • 29. 678 . Jette et al Physical Therapy . Volume 79 . Number 7 . July 1999 D ow nloaded from https://academ ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 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 func- tions as well, the ability to walk is poten- tially affected by factors such as reflex integrity, balance,10 depression,11 poor motor control,17,22 and endurance.3,16
  • 30. 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 volun- tary 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 Further- more, 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
  • 31. 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 dem- onstrating 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 categoriza- tion 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 associ-
  • 32. ation between muscle force and disability than between Figure 2. Distributions of percentage of predicted muscle force (%PMF) of lower-extremity movements according to walking ability in patients during the transition from walking with assistance in the community to walking only at home (n563). The dark line in the center of each box represents the median. The upper and lower bounds of each box represent the 75th and 25th percentiles, respectively. The lines extending from the boxes represent the highest and the lowest values that are not outliers. The circles represent values more that 1.5 box lengths from the highest or lowest values (outliers). Physical Therapy . Volume 79 . Number 7 . July 1999 Jette et al . 679 III III III III III III III III I D ow
  • 33. nloaded from https://academ ic.oup.com /ptj/article-abstract/79/7/672/2837094 by A P TA M em ber A ccess user on 18 M arch 2020 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 addi- tion, 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
  • 34. 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. Conclusion This study provides a profile of lower- extremity muscle force at critical tran- sitions in walking ability in patients with ALS. For each of the lower-extremity movements tested, there was a decrease in %PMF from the subject’s visit during which the walking function was at a higher level to the next visit during which the function was lower. The find- ings of our study provide support for a relationship between impairment and functional limitation and suggest possi-
  • 35. ble thresholds for lower-extremity mus- cle force required for various func- tional levels of walking. Wide variations in muscle forces within and between categories of walk- ing ability, however, suggest the difficulty of identifying force thresholds related to physical functions. References 1 Nagi SZ. Disability concepts revised: implications for prevention. In: Pope A, Tarlov A, eds. Disability in America: Toward a National Agenda for Prevention. Washington, DC: National Academy Press; 1991:193–203. 2 Verbrugge LM, Jette AM. The disablement process. Soc Sci Med. 1994;38:1–14. 3 Buchner DM, Cress ME, Esselman PC, et al. Factors associated with changes in gait speed in older adults. J Gerontol A Biol Sci Med Sci. 1996;51:M297–M302. 4 Chandler JM, Duncan PW, Kochersberger G, Studenski S. Is lower extremity strength gain associated with improvement in physical performance and disability in frail, community-dwelling elders? Arch Phys Med Rehabil. 1998;79:24 –30. 5 Damiano DL, Abel MF. Functional outcomes of strength training in spastic cerebral palsy. Arch Phys Med Rehabil. 1998;79:119 –
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