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Preservation of Directly Stimulated Muscle Strength in Hemiplegia Due to Stroke
William M. Landau, MD;
Shirley A. Sahrmann, PhD
Arch Neurol. 2002;59:1453-1457.
ABSTRACT
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Background Hemiplegia, or hemiparesis, severe impairment of purposeful activation
of striated musculature, is the most conspicuous and often most disabling
symptom of acute cerebrovascular lesions. Spontaneous improvement of voluntary
strength may extend over many months.
Objective In this archetypical upper motor neuron syndrome we wish to ascertain
the degree of functional impairment due to direct contractile impairment of
the affected striated musculature.
Design Maximal tetanic muscle contraction was elicited by electrical stimulation
applied directly to the tibialis anterior of the paretic and nonparetic limbs.
Maximal forces of the normal limbs were compared with the afflicted limbs
both early and late after vascular lesions of the pyramidal tract. Maximal
voluntary force of foot dorsiflexion in the same limbs was also determined.
Similar measurements were made in healthy control participants.
Setting Acute hospital, rehabilitation, and outpatient units of a clinical research
center.
Patients Patients with unilateral stroke were studied a few or many weeks after
the ictus.
Main Outcome Measures Comparison was made between contraction strengths induced by maximal
tetanic electrical stimulation of the dysfunctional and contralateral unaffected
muscles. Maximal voluntary strength of the foot dorsiflexion forces was also
measured.
Results Compared with the range of electrically evoked contractile force of
tibialis anterior between the limbs of healthy participants, the directly
elicited force in stroke-impaired tibialis anterior was not significantly
impaired.
Conclusions Modes of exercise therapy focused primarily on direct strengthening
of striated musculature, as in resistive exercise training, are strategically
questionable. Whether other approaches may be more effective remains to be
proved. The central disability of the upper motor neuron syndrome is failure
of rapid coordinated adjustment of graded high-frequency motoneuron firing
in purposeful complex synergies.
INTRODUCTION
THE MOST OBVIOUS impairment in patients with upper motor neuron syndrome
is compromise of limb movement that ranges in severity from mild clumsiness
to complete paralysis.1-5
The patients' limb "weakness," deficiency of foot dorsiflexion during walking,
and limited voluntary dorsiflexion, provide the rationale for conventional
rehabilitation strategy to strengthen the weak musculature.6-9
Thus, the innate presumption is that this disturbance is caused to a significant
degree by contractile deficiency of muscle, as may occur with myopathy or
peripheral denervation. Hence, the therapeutic approach is to have the patient
perform repetitive strengthening exercises, such as the training programs
that are used in sports medicine.6-7
Histologic studies10-16
have reported contractile tissue deficits and fiber type changes that support
the belief of contractile capacity impairments. Although Frontera et al16 described histologic changes in upper motor neuron
paretic muscles, they did not assess the deficiency of tension associated
with these changes. Other studies17-20
have shown that in stroke the impairment of voluntary strength is associated
with deficient motor unit recruitment and firing frequencies inadequate to
sustain tetanic muscle contraction. Patterns of muscle coordination are constrained
and distorted.21-23
Other investigators17, 24-26
have suggested that purposeful force of limb movement is significantly impaired
by spastic hyperactive stretch reflexes in antagonist muscles, but clear support
of this suggestion has not been provided.
Abnormalities of motoneuron activation thus compromise the voluntary
tension developed by muscle that could in turn affect the properties of the
contractile proteins. As is well established in muscle biology, the tension
demand on the muscle is the stimulus for adding or losing sarcomeres.27 The key question is whether the disturbed central
drive produces enough secondary effect on muscle to decrease contractile capacity.
If diminished muscular force is an important factor in hemiparesis, then methods
of improving muscle strength should be included in the rehabilitation program.
If not, other strategies need to be emphasized.
The purpose of this study was to assess whether the contractile capacity
of hemiparetic muscle in stroke patients is significantly different from that
of unaffected muscle. Because central recruitment of motoneuron activity is
impaired in affected limbs, electrical stimulation was used directly to assess
contractile capacity.
The loss of foot dorsiflexion at the ankle in hemiparesis is a central
feature of the upper motor neuron syndrome.1, 28-31
Deficiency of voluntary dorsiflexion and the drop-foot gait indicate that
the tibialis anterior (TA) is severely impaired during motions performed both
by conscious voluntary effort and by automatic central neural gait mechanisms.
Accordingly, the performance of TA was selected for analysis. Similar measurements
in control participants ascertained the normal range and symmetry of electrically
and voluntarily evoked forces.
PARTICIPANTS AND METHODS
Informed consent was obtained from 13 healthy control participants,
17 patients with acute hemiplegia or hemiparesis (disease duration, 1-7 weeks),
and 14 patients with chronic hemiplegia or hemiparesis (disease duration,
25-624 weeks) (Table 1). All patients
had acute hemiplegia or hemiparesis resulting from cerebral hemispheric infarction
or hemorrhage, with one exception (acute patient 6, Table 1, had infarction of the medullary pyramidal tract). All brain
lesions had been confirmed by computed tomography or magnetic resonance imaging
. All had increased tendon jerks in the hemiparetic limbs. Not all had clasp-knife
spasticity or extensor plantar reflexes. Calf muscle atrophy (maximal circumference,
at least 1.0 cm less than the normal leg) was observed in only 1 patient (chronic
patient 13, Table 1). However,
TA atrophy was not otherwise evident by clinical inspection and palpation.
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Characteristics of the Study Sample*
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Patients with acute disease were in the hospital neurorehabilitation
unit (12 men, 5 women; age range, 47-99 years). The patients with chronic
disease were living at home (7 men, 7 women; age range, 48-78 years). Patients
with bilateral lesions or impaired capacity for cooperation and consent due
to aphasia or dementia were not included. The control participants were healthy
volunteers without evident neurologic impairment (3 men, 10 women; age range,
24-72 years). None had cerebral imaging procedures.
Participants were seated in a padded chair so that the hip and knee
of the extremity to be tested were flexed to 90°. The sock-covered foot
was strapped tightly with a 5-cm nylon strap to a flat metal footplate with
the foot in 10° of plantar flexion. The isometric torque force of dorsiflexion
was sensed by a strain gauge fixed to a rigid metal block that was attached
in parallel to the footplate with its axis proximal to the heel. Strain gauge
voltage was acquired and analyzed using the Spike 2 Cambridge University computer
program (Cambridge Electronic Components, Cambridge, England).
The skin over the tested anterior upper part of the leg was wiped dry
with alcohol sponges; the lateral tibial margin was then palpated and marked
with ink so that the conductive adhesive pads (Versa-Stim; Electromed, Miami,
Fla) could be uniformly situated 0.5 cm from the bony edge. These electrodes
were 7 cm long, 4.5 cm wide, and 1 cm apart. The upper pad was trimmed to
fit the curve of the upper tibial origin of the TA (Figure 1). The combined electrode resistance ranged from 47 to 60  .
The Versa-Stim 380 (Electromed) constant current stimulator delivered 10-millisecond
duration, 2.5-kHz sine wave bursts at the rate of 50 per second. This instrument
was used because it was specifically designed to deliver a high-intensity
stimulus that was comfortable for use in rehabilitation. As anticipated, we
found good subjective tolerance of a 1.5-second duration stimulus, including
a 0.4-second ramp rise to steady current. The routine was to deliver three
1.5-second stimulus bursts at 2-second intervals followed by a minimal 2-minute
rest, which provided good recovery of force between stimulus epochs. As the
stimulus intensity was gradually increased, the subject first reported a buzzing
tactile cutaneous sensation, then a painless muscle shortening. The strongest
intensities were perceived as brief painful muscle cramps.
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Figure 1. Diagram of stimulating electrode
placement.
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Stimulus intensity was increased stepwise until the generated force
reached a plateau for several increments or began to decrease. After a rest,
the subject was instructed to dorsiflex the foot maximally at the ankle 3
times at 2-second intervals. These contractions ranged from 1 to 3
seconds. The patient's unaffected limb was always tested first. The largest
force generated by electrical stimulation (stimulus maximal force [StMF])
or voluntary effort (voluntary maximal force [VoMF]) was used for data analysis.
RESULTS
Muscular size and strength along with sex and age varied widely among
both the patients and the control participants (Table 1). Among the healthy participants, the StMF elicited from
the TA ranged from 32 to 235 newtons (N). To compare the data statistically
and graphically, the original force numbers for each subject were normalized
(Figure 2, Figure 3, and Figure 4)
and the data are presented as mean (SD). For the control participants, the
maximal response to electrical stimulation of each left TA was arbitrarily
set at 100% as the reference standard for the other direct force measurements
in the same subject (Figure 2).
Thus, the mean StMF in the right TA of the healthy participants was 96% (SD,
29%) of the left.
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Figure 2. Graphic presentation of maximal
force data for healthy control participants. Vol indicates conscious forceful
effort; stim, tetanic electrical stimulation of the tibialis anterior. The
numbers inside the figure represent the individual participants identified
in Table 1.
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Figure 3. Graphic presentation of maximal
force data for patients with acute hemiplegia or hemiparesis. NPV indicates
nonparetic limb, conscious forceful effort; NPST, nonparetic limb, tetanic
electrical stimulation of the tibialis anterior; PST, paretic limb, tetanic
electrical stimulation of the tibialis anterior; and PV, paretic limb, conscious
forceful effort. The numbers inside the figure represent the individual participants
identified in Table 1.
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Figure 4. Graphic presentation of maximal
force data for patients with chronic hemiplegia or hemiparesis. NPV indicates
nonparetic limb, conscious forceful effort; NPST, nonparetic limb, tetanic
electrical stimulation of tibialis anterior; PST, paretic limb, tetanic electrical
stimulation of tibialis anterior; and PV, paretic limb, conscious forceful
effort. The numbers inside the figure represent the individual participants
identified in Table 1.
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The VoMF of foot dorsiflexion was much larger than the StMF because
TA was reinforced by extensor digitorum longus, extensor hallucis longus,
and peroneus tertius. For the control subjects (Figure 2), with reference to each participant's left StMF, the average
left VoMF was 259% (range, 141%-398%) and on the right the mean VoMF was 249%
(range 134%-408%). The mean difference between normal left and right VoMFs
was 29% (SD, 22%) of the reference left StMF. With the premise that both electrically
induced and voluntary forces should be symmetrical in healthy participants,
these data are the measure of experimental range of our methods.
The patients in our early stroke group (Table 1; Figure 3) were
examined 1 to 5 weeks after the stroke. The StMF of the unaffected limb (NPST)
served as the 100% reference standard; among 17 patients, these forces ranged
from 21 to 209 N. To our surprise, the mean StMF of the affected limbs (PST)
was larger, 126% (SD, 48%). The paired t test value
between limbs was just significant (2.16; P = .045).
The patients with chronic stroke (Table 1; Figure 4) were
studied between 25 and 437 weeks after the ictus. The 100% reference StMF
forces of the unaffected extremity (NPST) ranged from 31 to 308 N. There was
still a trend for the PST to be larger in the affected TA, mean 118% (SD,
60%; paired t test, 1.1; P
= .30, not significant). The PST of chronic patient 13 (Table 1), the only patient with definite calf muscle atrophy, was
135% of the reference NPST. This patient was also the only one with chronic
disease whose voluntary paralysis of TA remained complete.
For the early patient group (Figure
3), the mean VoMF of the unaffected limbs (NPV) was 311% (SD, 115%).
The mean VoMF of the affected limbs (PV) was less than a third of this magnitude,
90% (SD, 81%). The mean difference between unaffected and affected limb VoMFs
was 221% (SD, 145%). For the patients with chronic disease (Figure 4), the mean VoMF of the unaffected limb (NPV) was 278% (SD,
143%) and for the paretic limb (PV) 171% (SD, 166%). The mean difference between
individual unaffected and affected limb VoMFs was 107% (SD, 102%). Of course,
these were not the same patients, but the mean degree of voluntary paresis
in the chronic group had recovered to about half that of the acute group.
COMMENT
With electrical stimulation, the active musculature is the artificial
and relatively restricted product of our best practical effort to produce
equivalent electrical fields in the regions just lateral to the tibiae and
accurately to duplicate the force measurement setups in both limbs. We presume
that with an increasing stimulus current the StMF reaches a plateau when the
electrical field becomes sufficiently broad and intense to activate the entire
TA. We suspect that decreasing dorsiflexor force beyond the maximum signals
that current has spread to the peroneus longus, whose action is to plantar
flex and evert the foot. In many participants, this eversion could be readily
seen.
High-frequency motor unit firing and consequent tetanic muscle contraction
is the necessary pattern for strong purposeful movement. Theoretically, tetanic
stimulation of the isolated TA motor nerve would be a more precise technique,
but preliminary experiments showed that pain makes the procedure intolerable
for unanesthetized human participants. The degree of discomfort produced by
direct muscle stimulation was readily accepted by all of our participants.
The range of asymmetry between the 2 limbs of our healthy participants represents
both physiologic and instrumental factors (eg, imperfect symmetry of electrode
placements).
We have no obvious explanation for the slightly larger StMF in the paretic
TA muscles of our patients, a finding that was statistically significant in
the early stages. For those patients whose paretic TA StMF was smaller than
the nonparetic, we cannot exclude the possibility of a small element of decreased
contractility of the muscle tissue.
Nevertheless, we believe that these data support the conclusion that
true failure of contractile muscle force competence following stroke is not
a major factor in the common gait and other functional deficits of hemiparesis.
Both early and late after the lesion, and even with fairly good recovery of
purposeful foot dorsiflexion, the primary manifestation of hemiparesis is
impaired initiation and coordination. Although slight atrophy may occur, this
contrasts with the gross weakness and atrophy that characterizes motoneuron
or muscle disease. With higher-level lesions (Jackson's middle level and Gowers'
upper motor neuron), movement dexterity and repertory are conspicuously impaired
relative to force.28, 32-33
Of course, both purposeful voluntary force and improved gait coordination
almost always increase following stroke, with or without formal physical therapy.
Evidently this improvement is accomplished by recruitment of more motoneurons
and by increased motor unit firing rates that produce tetanic muscle contraction.
Whether this central nervous system recovery is improved or best improved
by instructed voluntary effort focused upon strength is empirically uncertain.
Our extended suggestion from these observations in stroke is that the
symptom usually labeled as weakness by patients with primary brain disease
does not represent a major pathophysiologic disturbance of muscle tissue.
Also likely, but unproved, is the hypothesis that impaired persistence and
pattern of activation of final common path motoneurons account for the operational
"weakness" in cerebral palsy, multiple sclerosis, parkinsonism, and other
encephalopathies that affect motor performance.34-35
Of course, primary voluntary effort may be decreased by associated pain and
is decreased in somatization syndromes.
In stroke, the conceptual basis of therapeutic approaches should be
directed toward correcting the retarded, diminished, and interfering patterns
of central nervous system malfunction rather than toward the striated musculature,
which serves only as the peripheral end organ that generates force. Whether
particular adaptive instructional programs can improve upon spontaneous recovery
from acute upper motor neuron impairment remains to be proved.36-43
AUTHOR INFORMATION
Accepted for publication April 18, 2002.
Author contributions: Study
concept and design (Drs Landau and Sahrmann acquisition
of data (Drs Landau and Sahrmann); analysis and interpretation
of data (Drs Landau and Sahrmann );drafting of the
manuscript (Drs Landau and Sahrmann); critical revision
of the manuscript for important intellectual content (Drs Landau and
Sahrmann); statistical expertise (Dr Sahrmann); obtained funding (Dr Landau); administrative, technical, and material
support (Drs Landau and Sahrmann); study supervision (Drs Landau and Sahrmann).
We thank Thomas Thach, MD, and Jonathan Mink, MD, PhD, for lending us
their recording equipment and Phyllis Lehman, BA, of Electromed for her help
in adapting the Versa-Stim apparatus to our purpose. Margaret Clare Griffin,
MA, collaborated in our preliminary experiments.
Corresponding author and reprints: William M. Landau, MD, Department
of Neurology, Washington University School of Medicine, 660 South Euclid Ave,
St Louis, MO 63110 (e-mail: landauw{at}neuro.wustl.edu).
From the Department of Neurology (Drs Landau and Sahrmann) and Program
in Physical Therapy (Dr Sahrmann), Washington University School of Medicine,
St Louis, Mo.
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