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ORIGINAL ARTICLE
The purpose of the this study was to investigate, in vivo and trocnemius muscle. The motor at the knee was fixed rigidly to
noninvasively, the biomechanical changes of the medial gas- a frame anchored to the ground, and a leg linkage was mounted
trocnemius muscle at both the joint level (characterized by the to the knee motor through a 6-axis JR3 force sensor.a The ankle
ROM, stiffness, resistance torque at controlled position) and motor was mounted at the distal end of the leg linkage, and a
the muscle fascicle level (characterized by the muscle fascicle footplate was mounted to the ankle motor through another
length, pennation angle, muscle thickness) at ankles in both 6-axis force sensor. The ankle motor and footplate could be
stroke survivors with spasticity/contracture and healthy control adjusted along the leg linkage so that the ankle and knee motors
subjects. We hypothesized that there are significant differences were aligned with the ankle and knee flexion axes, respectively
in these biomechanical properties at the fascicle and joint levels (fig 1).
between the 2 groups, and changes at the joint level are
correlated to those at the fascicle level. Experimental Protocol
A brief medical history including the date of stroke, ambu-
METHODS latory status, use of ankle-foot orthosis, use of antispasticity
drugs, and current therapy was documented for each stroke
Participant Selection survivor. The leg length (from the lateral femoral epicondyle to
A convenience sample of 10 chronic stroke survivors (at the lateral malleolus19) and foot height (from the bottom of foot
least 1 year poststroke; age, 54.7⫾11y; weight, 84.5⫾15.5kg; to the lateral malleolus) were measured to align the knee and
height, 176⫾5.3cm; shank length, 39.4⫾1.0cm) with ankle ankle with the experimental device.
spasticity/contracture were recruited. The Modified Ashworth Subjects were seated upright with the thigh and trunk se-
Score18 was measured at the ankle (2.57⫾0.58). In addition, cured using Velcro straps. The leg and foot were attached to the
the following criteria were used: the subjects were not involved leg linkage and footplate, respectively (see fig 1). Four knee
in any other studies that could potentially affect the test results, positions, starting from full extension with an increment of 30°
and subjects could walk independently without walking aid and of flexion, were tested. At each knee position, the ankle flexion
sit on a chair for 2 hours. Ten age-matched and sex-matched angle was systematically varied between 20° dorsiflexion and
healthy subjects (age, 56.6⫾20.7y; weight, 87.1⫾17.6kg; 45° plantar flexion, with increments of 10° in dorsiflexion and
height, 177.3⫾3.7cm; shank length, 38.6⫾1.2cm) without any 15° in plantar flexion relative to 0° of ankle flexion. The knee
neurologic or muscular disorders served as controls. All sub- and ankle motors were locked at each of the target positions. At
jects gave informed consent approved by the institutional re- each knee position, the subject was asked to relax with the
view board. ankle at the resting position. The corresponding ankle resting
angle and torque were recorded. In addition, the resistance
Experimental Setup torque at 0° dorsiflexion was measured. At each of the knee and
A custom knee-ankle joint test device was used to investi- ankle positions, the subject was asked to relax, and the knee
gate the biomechanic properties of the biarticular medial gas- and ankle torques and angles were recorded for 2 seconds.
Fig 1. (A) Experimental setup. The knee-ankle evaluation device consists of 2 motors and a linkage between. The JR3 force/torque sensors
were mounted on the motor shaft at both joints to measure the joint torques/forces. With the knee flexion axis aligned with the knee motor,
the ankle motor can be adjusted along the leg linkage to align it with the ankle flexion axis. (B) Longitudinal ultrasonic images of the medial
gastrocnemius muscle at rest. The skin is on the top of the image, and the left side corresponds to proximal. The muscle tendon junction
represented the musculo-tendon (muscle aponeurosis) junction. ␣ and  are the posterior and anterior pennation angles, respectively. The
medial gastrocnemius muscle tendon junction was taken as the distal reference point.
Because some stroke survivors had reduced ROM, the exper- mius fascicular stiffness was determined as the slope of the
iment was conducted within the comfort limits of each subject. medial gastrocnemius fascicular force and fascicular length
Ultrasonic images of the medial gastrocnemius muscle were relationship.
collected using a 14-MHz high-resolution matrix probe.b
LOGIQView, a technique of extended field of view, was used Statistical Analysis
to overcome the limited field of view and register the muscle Repeated-measures analysis of variance was used to analyze
images covering the full fascicle lengths. A previous study has the response variables (fascicle length, pennation angles, mus-
shown the reliability of ultrasound technique for measuring cle thickness, joint stiffness, ROM) with respect to each factor
muscle architecture,20 and the accuracy of extended field of (subject population, ankle position, knee position). The signif-
view has been reported to be better than 5%.21 The probe was icance level was set at .05, and adjustments were made if a
placed perpendicular to the skin and moved smoothly along the violation of sphericity was found (Huynh-Feldt adjustment if
middle line of the medial gastrocnemius throughout its length the sphericity estimate ⬎0.75, Greenhouse-Geisser otherwise).
(see fig 1). All scans were conducted by an experimenter with The Student t test was used for comparison of the variables
experience in ultrasonic measurements. The scan was repeated between groups. The Pearson correlation coefficient was used
3 times, and the averaged values of these measurements across to quantify associations among the variables, and the Spearman
scans were used in further analysis. rank correlation was used to test the monotonic trend (eg, if one
variable is increased, the other follows). Correlations between
the muscle architecture measures (medial gastrocnemius fas-
Data Analysis cicular stiffness, fascicle length, pennation) and the joint-level
The torque signal at each joint was low-pass–filtered with variables (passive resistance torque, joint stiffness, ankle dor-
fourth-order Butterworth filter (5Hz cutoff frequency) and av- siflexion ROM) were evaluated.
eraged across the 2-second period. Ankle joint stiffness was
calculated as the change of ankle joint resistance torque over RESULTS
the change of ankle joint angle (K⫽⌬/⌬) across the ROM. In
this study, the ankle joint stiffness was quantified between Biomechanic Changes at the Joint Level
different ankle positions reaching steady state instead of during Decreased passive ankle range of motion in stroke survi-
continuous dynamic movement. The muscle fascicle length,22 vors. Under comparable joint torques (5Nm in dorsiflexion
as indicated by the line between the aponeuroses, was mea- and 3Nm in plantar flexion), stroke survivors showed reduced
sured at 5cm proximal to the muscle-tendon junction (see fig ROM compared with healthy controls. With knee flexion of
1B). In addition to the absolute fascicle length, its normaliza- 30°, the ankle positions ranged from –34.1⫾4.8° to –3.1⫾4.1°
tion to the lower-leg length was also calculated for the indi- and from –37.7⫾4.8° to 13.5⫾6.9° for stroke survivors and
vidual subjects. The pennation angle was defined as the angle healthy control groups, respectively. The ROM difference be-
between the fascicle and the aponeurosis both posteriorly and came significant as the ankle was dorsiflexed. The ankle posi-
anteriorly (see fig 1B). For simplicity, we focused on the tions ranged from –31.2⫾7.9° to – 6.4⫾5.1° and from
anterior pennation angle. Muscle thickness was measured at –35.3⫾6.5° to 6.5⫾5.3° with the knee fully extended for
5cm proximal from the muscle-tendon junction (see fig 1B). stroke survivors and healthy control groups, respectively.
Measurements including joint resistance torque, joint stiffness, Across the different knee flexion angles, patients poststroke
muscle fascicle length, and pennation angle were interpolated showed a larger ankle resting angle (more into plantar
across the ankle flexion using the shape-preserving piecewise flexion) than the healthy controls (P⫽.006). At full knee
cubic method (by using interp1 function in MATLAB with extension, the ankle resting positions of the stroke and healthy
option pchipc). groups were –18.2⫾6.6° and –13.6⫾3.9°, respectively. With
The gastrocnemius contribution to the ankle passive resis- the knee flexed from 30° to 90°, the resting positions changed
tance torque was estimated as the difference of the passive from 19.5⫾5.2° to 17.5⫾4.6° and from 12.7⫾3.5° to
ankle resistance torque between full knee extension and 90° 13.1⫾5.2° for the stroke and control groups, respectively.
knee flexion. The calculation was done in the range of 20° Although the medial gastrocnemius spans both knee and ankle,
plantar flexion to 15° dorsiflexion. With the gastrocnemius the ankle resting position was not significantly affected by the
moment arm for ankle plantar flexion obtained from SIMM,d knee position (P⫽.841).
the passive resistance force of the gastrocnemius was deter- Increased ankle stiffness in stroke survivors. Ankle stiff-
mined and related to the measured medial gastrocnemius fas- ness changed with both ankle (P⬍.001) and knee flexion
cicle length. The moment arm was not normalized for individ- (P⬍.001). Stroke survivors exhibited higher ankle stiffness
ual subjects because there were no significant differences in than healthy controls, especially in dorsiflexion (fig 2; P⬍.05).
body height for either stroke survivors (P⫽.15, t test) or At 0° dorsiflexion and full knee extension, for example, the
healthy controls (P⫽.74, t test) compared with the body height stiffness was .24⫾.08 and .72⫾.28Nm/° for the control and
used in SIMM (175cm, height of an average man). Further- stroke groups, respectively. Ankle stiffness ranged from .076 to
more, assuming the passive force sharing between the lateral .75Nm/° and from .17 to 1.46Nm/° for the control and stroke
and medial heads of gastrocnemius to be proportional to the groups, respectively. Ankle stiffness was highest at extreme
ACSA with the medial and lateral gastrocnemius ACSAs at dorsiflexion and lowest around the ankle resting position (see
10.20 and 6.53cm2, respectively,23 the passive medial gastroc- fig 2).
nemius force was determined as 61% of the total passive
gastrocnemius force. It was assumed that the passive tension of Biomechanic Changes at the Muscle Fascicle Level
the gastrocnemius muscle was negligible at 90° knee flexion
because it had been reported that the passive tension was close Muscle fascicle length. As a biarticular muscle, the medial
to 0 with 10° plantar flexion and greater than 50° knee flex- gastrocnemius muscle fascicle length varied with both ankle
ion.24 The corresponding medial gastrocnemius fascicular (P⫽.001) and knee flexion (fig 3; P⫽.001, both groups com-
force was scaled by 1/cos(pennation), with pennation the penna- bined), and a significant interaction between the knee and ankle
tion of medial gastrocnemius fascicles. The medial gastrocne- flexions was also observed (Pⱕ.001). The fascicle length in-
creased monotonically as the ankle dorsiflexed but decreased as angle increased from 19.5⫾2.6° to 27.4⫾5.1° as the knee
the knee flexed (Pⱕ.001; see fig 3). For instance, for stroke flexed from 0° to 90° flexion with the ankle at 0° dorsiflexion
survivors, the muscle fascicle length increased from 32.0⫾ (fig 4). The pennation angle ranged from 17.1⫾2.4° to
8.1mm to 58.8⫾10.7mm as the ankle moved from 45° plantar 41.4⫾7.8° and from 14.2⫾4.0° to 37.1⫾6.4° for the healthy
flexion to 15° dorsiflexion with the knee at full extension, while and stroke groups, respectively.
it decreased from 51.4⫾8.4mm to 34.2⫾7.0mm as the knee Stroke survivors showed smaller pennation angles than
flexed from full extension to 90° flexion with the ankle at the healthy controls, especially at more extended knee positions
neutral position. (Pⱕ.049; fig 5). For instance, the pennation angles with the
Although the 2 groups showed similar trends, stroke survi- ankle at 0° dorsiflexion and at 30° of knee flexion were
vors had significantly shorter muscle fascicles compared with 22.1⫾3.1° and 17.5⫾3.9° for the controls and stroke survivors,
healthy subjects across the ankle ROM, especially with the
respectively. The differences decreased as the ankle ap-
ankle dorsiflexed (see fig 3; P⬍.05). Medial gastrocnemius
fascicle length depended on both knee and ankle positions, and proached extreme dorsiflexion.
significant interaction between the 2 joints was observed Muscle thickness. With the knee extended and/or the ankle
(P⬍.05). With the knee fully extended, for example, the fas- dorsiflexed, the medial gastrocnemius became tighter, and
cicle length of stroke survivors was shorter than that of healthy muscle thickness decreased. As the knee was flexed, the change
controls across the range of 45° plantar flexion to 15° dorsi- in muscle thickness with ankle dorsiflexion also increased. For
flexion. However, the difference diminished as the knee was instance, for healthy control subjects, as the ankle moved from 15°
flexed. Similar results were observed for normalized muscle dorsiflexion to 45° plantar flexion, the muscle thicknesses in-
fascicle lengths. Stroke survivors showed significantly shorter creased from 10.0⫾3.7 to 15.0⫾3.1mm, 9.8⫾4.0 to 14.7⫾
normalized muscle fascicle length than healthy controls, espe- 2.8mm, 10.7⫾3.2 to 16.2⫾2.5mm, and 10.9⫾2.6 to 17.6⫾
cially with the ankle dorsiflexed (P⬍.05). 3.5mm at 0°, 30°, 60°, and 90° knee flexion, respectively.
Pennation angle. The pennation angle decreased mono- The muscle thickness for stroke survivors was slightly
tonically as the ankle moved from plantar to dorsiflexion and smaller than that of healthy controls. However, the differ-
increased as the knee flexed from full extension to 90° flexion ences were significant only at extreme ankle dorsiflexion
(P⫽.001). For instance, for control subjects, the pennation and knee extension.
Passive force and fascicle length relationship. At compa- angle (r⫽.304; P⬍.01) and medial gastrocnemius muscle fas-
rable levels of medial gastrocnemius fascicular force, ranging cicle stiffness (r⫽–.151; P⬍.05) at full knee extension. Joint
from 20 to 80N, the medial gastrocnemius fascicular stiffness stiffness showed a negative correlation with muscle fascicle
(slope of the medial gastrocnemius fascicular force and medial length (r⫽–.20; P⬍.01) and a positive correlation with medial
gastrocnemius fascicular length relationship) was significantly gastrocnemius fascicular stiffness (r⫽.51; Pⱕ.001). Signifi-
higher for stroke survivors than controls (Pⱕ.044; see fig 4). cant correlations were observed between the variables evalu-
For example, at 50N medial gastrocnemius fascicular force, the ated within the fascicle or joint level. At the fascicle level,
slopes were 12.4⫾4.7 and 6.5⫾3.6N/mm for the stroke and muscle fascicle length was correlated with pennation angle
control groups, respectively. Similarly, the gastrocnemius force (r⫽–.46; Pⱕ.001). At the joint level, the resistance torque and
and medial gastrocnemius fascicle length curve of stroke sur- joint stiffness were correlated (r⫽.66; Pⱕ.001), and the 2
vivors had significantly steeper slope than that of controls at
variables were both correlated with the ankle ROM negatively
comparable levels of gastrocnemius force (Pⱕ.044). In addi-
tion, at comparable gastrocnemius passive tension levels rang- (r⫽–.69, Pⱕ.001; and r⫽–.38, Pⱕ.001, respectively).
ing from 30 to 130N, stroke survivors had significantly shorter
medial gastrocnemius fascicle length than controls (Pⱕ.025). DISCUSSION
For instance, the medial gastrocnemius muscle fascicle lengths Biomechanic changes at the ankle joint are associated with
were 48.1⫾13.4 and 65⫾15mm for the stroke and control spasticity/contracture in stroke survivors, including reduced
groups, respectively, at 80N gastrocnemius passive tension ROM and increased resistance and stiffness at the ankle. How-
(Pⱕ.001; see fig 4). ever, the corresponding changes at the muscle fascicle level
and the correlations between changes at the 2 levels have not
Relationship Between Changes at the Joint and Fascicle been investigated together in the stroke population. In this
Levels study, we use ultrasonography combined with biomechanical
The joint and fascicle level variables were correlated. The measurements to evaluate in vivo muscle fascicle as well as
ankle ROM showed a moderate negative correlation with joint properties and correlate the pathologic changes at the joint
the muscle fascicle length (r⫽–.286; P⬍.01), pennation level with the underlying changes at the muscle fascicle level.
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