You are on page 1of 8

819

ORIGINAL ARTICLE

Changes in Passive Mechanical Properties of the


Gastrocnemius Muscle at the Muscle Fascicle and Joint Levels
in Stroke Survivors
Fan Gao, PhD, Thomas H. Grant, MD, Elliot J. Roth, MD, Li-Qun Zhang, PhD
ABSTRACT. Gao F, Grant TH, Roth EJ, Zhang L-Q. Key Words: Contracture; Muscle spasticity; Rehabilitation;
Changes in passive mechanical properties of the gastrocnemius Stroke.
muscle at the muscle fascicle and joint levels in stroke survi- © 2009 by the American Congress of Rehabilitation
vors. Arch Phys Med Rehabil 2009;90:819-26. Medicine
Objectives: To investigate the ankle joint–level and muscle
fascicle–level changes and their correlations in stroke survivors PASTICITY, CONTRACTURE, and muscle weakness are
with spasticity, contracture, and/or muscle weakness at the
ankle.
S commonly observed after stroke and are major sources of
disabilities poststroke. Clinically, the phenomenon of footdrop
Design: To investigate the fascicular changes of the medial is associated with an increase in the tone of the calf muscles.
gastrocnemius muscle using ultrasonography and the biome- Muscle tone may result from both reflex and nonreflex changes
chanical changes at the ankle joint across 0°, 30°, 60°, and 90° and is usually accompanied with increase of passive joint/
knee flexion in a case-control manner. muscle stiffness.1 In the spastic lower limb, it is not clear how
Setting: Research laboratory in a rehabilitation hospital. hypertonia at the ankle joint is related to changes in the
Participants: Stroke survivors (n⫽10) with ankle spasticity/ biomechanical properties of the plantar flexor muscles.2-7 A
contracture and healthy control subjects (n⫽10). better understanding of changes in muscle architecture and its
Interventions: Not applicable. association with joint biomechanical properties could help us
Main Outcome Measurements: At the muscle fascicle gain insight into mechanisms underlying spasticity/contracture
level, medial gastrocnemius muscle architecture including the and provide guidance to the rehabilitation of patients post-
fascicular length, pennation angle, and thickness were evalu- stroke. The changes in the mechanical properties may be as-
ated in vivo with the knee and ankle flexion changed system- sociated with changes in skeletal muscle architecture, such as
atically. At the joint level, the ankle range of motion (ROM) muscle fascicle length, pennation angle, and muscle thickness.
and stiffness were determined across the range of 0° to 90° Muscle architecture plays a significant role in normal muscle
knee flexion. function and is closely related to the mechanical properties of
Results: At comparable joint positions, stroke survivors the joint.8 Recent studies based on a biomechanical model
showed reduced muscle fascicle length, especially in ankle suggested that an increase in ankle joint stiffness could be
dorsiflexion (Pⱕ.048) and smaller pennation angle, especially attributed to shortened calf muscles.2 However, there has been
for more extended knee positions (Pⱕ.049) than those of little experimental evidence evaluating muscle architecture and
healthy control subjects. At comparable passive gastrocnemius joint stiffness in the same patients with ankle spasticity/con-
force, stroke survivors showed higher fascicular stiffness tracture.
(Pⱕ.044) and shorter fascicle length (Pⱕ.025) than controls. Ultrasonography has been used in studying muscle and ten-
The fascicle-level changes of decreased muscle fascicle length don function in healthy populations in vivo and noninva-
and pennation angle and increased medial gastrocnemius fas- sively.9-11 However, only a few ultrasonic studies have been
cicle stiffness in stroke were correlated with the joint level conducted to examine hypertonic muscles in patients with
changes of increased joint stiffness and decreased ROM neurologic disorders, with mixed results reported and with a
(P⬍.05). lack of study on lower limb muscle architecture poststroke.
Conclusions: This study evaluated specific muscle fascicu- Shortland et al12 reported no difference in muscle fascicle
lar changes as mechanisms underlying spasticity, contracture, length between children with spastic diplegia and healthy chil-
and joint-level impairments, which may help improve stroke dren, suggesting muscle architecture changes do not contribute
rehabilitation and outcome evaluation. to contracture in the patients, while Cheatwood et al13 reported
significantly shorter muscle fascicle length in the group of
children with spastic cerebral palsy. Li et al14 found that the
fascicle length of spastic brachialis muscle on the affected side
was significantly shorter than that on the unimpaired side. The
From the Rehabilitation Institute of Chicago, Chicago, IL (Gao, Roth, Zhang);
Departments of Physical Medicine and Rehabilitation (Gao, Roth, Zhang), Orthopae- differences in gastrocnemius muscle architecture were also
dic Surgery (Zhang), Biomedical Engineering (Zhang), and Radiology (Grant), North- studied in children with cerebral palsy, and fascicle length of
western University, Chicago, IL; Department of Health and Kinesiology, University spastic muscle was significantly shorter than that in nonparetic
of Texas at Tyler, Tyler, TX (Gao). muscle of healthy children.15-17
Supported by the National Institutes of Health (grant nos. HD044295 and
HD043664).
No commercial party having a direct financial interest in the results of the research
supporting this article has or will confer a benefit on the authors or on any organi-
zation with which the authors are associated. List of Abbreviations
Reprint requests to Li-Qun Zhang, PhD, Rehabilitation Institute of Chicago, Ste
1406, 345 E Superior St, Chicago, IL 60611, e-mail: l-zhang@northwestern.edu. ACSA anatomical cross-sectional area
0003-9993/09/9005-00495$36.00/0 ROM range of motion
doi:10.1016/j.apmr.2008.11.004

Arch Phys Med Rehabil Vol 90, May 2009


820 FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao

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.

Arch Phys Med Rehabil Vol 90, May 2009


FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao 821

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-

Arch Phys Med Rehabil Vol 90, May 2009


822 FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao

Fig 2. Passive stiffness at the


ankle joint for both healthy
subjects (dark line) and pa-
tients poststroke (gray line) at
4 knee positions: (A) full knee
extension, (B) 30° knee flex-
ion, (C) 60° knee flexion, and
(D) 90° knee flexion. *Signifi-
cant differences between the 2
populations with P<.05 (t test).
Abbreviations: DF, dorsiflexion;
PF, plantarflexion.

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.

Arch Phys Med Rehabil Vol 90, May 2009


FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao 823

Fig 3. Muscle fiber lengths of


both healthy subjects (dark
line) and stroke survivors
(gray line) at 4 knee positions:
(A) full knee extension, (B) 30°
knee flexion, (C) 60° knee flex-
ion, and (D) 90° knee flexion.
*
Significant differences be-
tween the 2 populations with
P<.05 (t test). Abbreviations:
DF, dorsiflexion; PF, plantar-
flexion.

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.

Arch Phys Med Rehabil Vol 90, May 2009


824 FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao

the smaller pennation angles in stroke survivors observed in


this study indicated muscle atrophy poststroke. Furthermore,
considering the muscle fascicle length may be reduced post-
stroke, the decreased pennation angle suggests higher fascicu-
lar tension under the passive condition, which may be associ-
ated with the increased tone of the calf muscles in stroke.
Functional impairments at the joint level are closely related
to the changes in muscle architecture properties. The higher
medial gastrocnemius fascicle stiffness, joint stiffness in dor-
siflexion, and reduced ROM at controlled resistance torques in
stroke survivors were associated with shortening of muscle
fascicles as demonstrated by the significant correlations be-
tween the 2 sets of variables. It has been shown that the number
of sarcomeres in series in a muscle is highly adaptable to
changes in muscle length.30-32 Patients poststroke often de-
velop footdrop, which may be a result of shortened plantar
flexors fascicles. As shown in figure 4, stroke survivors had
significantly higher gastrocnemius muscle and medial gastroc-
nemius fascicular stiffnesses, indicating an underlying mecha-
nism for the increased joint stiffness. This was consistent with
an in vitro study by Friden and Lieber,33 who showed that the
spastic muscle cell is stiffer and shorter than the normal con-
Fig 4. The relationship between the medial gastrocnemius fascicle trol. Similarly, through modeling analysis, Svantesson et al34
length and the passive gastrocnemius force (thick line) and the showed that muscle stiffness was significantly higher in the
medial gastrocnemius fascicle force (gastrocnemius force ⴛ 0.610 / affected leg than the nonaffected leg of stroke survivors. In
cos(␪pennation); thin line) for the stroke and control groups (the group addition, in this study, a significant correlation (r⫽.855;
average with 1-sided SE was shown for both fascicle length and
muscle/fascicle force). The medial gastrocnemius fascicle length P⬍.001) was observed between the Modified Ashworth Score
was determined at full knee extension with ankle between 20° and ankle joint stiffness.
plantar flexion and 15° dorsiflexion.
Study Limitations
There were limitations with the present study. First, the
fascicle length and pennation were determined 5cm from the
The current study examined biomechanic changes at the muscle tendon junction. Although it has been shown that there
joint level with more complete knee-ankle positions than pre- is marked uniformity in fascicle length throughout a mus-
vious studies on healthy subjects.2,4,7 In the current study, 4 cle,35,36 some studies reported heterogeneity of pennation an-
knee positions ranging from full extension to 90° flexion were gles37 and fascicle lengths38 along the length of muscle. Thus,
evaluated, while previous studies usually involved only 1 knee the relationships between joint angles and fascicle arrangement
position,4,7 and 1 study measured changes in gastrocnemius might differ in different portions of a muscle. In this study, we
fascicle length as a function of knee and ankle position without chose the location of 5cm from the muscle tendon junction to
reporting the absolute fascicle length.25 Our results agreed well obtain a representative measurement and kept it consistent
with previously reported results at comparable leg posi- across the subjects. Second, the measured medial gastrocne-
tions.2,4,7 For instance, the ankle joint stiffness measured at mius pennation angle was assumed to be the same for the
10° dorsiflexion with 90° knee flexion for stroke survivors lateral gastrocnemius. However, the lateral head may have
was 0.6⫾0.4Nm/° in the current study and 0.5⫾0.4Nm/°,7 smaller pennation.10 To distribute the tension between the
0.44Nm/°,2 and 0.5⫾0.4Nm/°4 in previous studies. lateral and medial heads, we assumed that the tension was
In this study, muscle architecture was compared between proportional to the ACSA, which represented an approximation
stroke survivors and healthy subjects quantitatively. In general, for the 2 populations. It would be interesting to see whether the
measurements of muscle architecture in healthy subjects agreed ACSA and passive tension ratio of medial head to lateral head
well with previously published data.10,20,25-28 In this study, the is altered because of stroke. Last, the sample size in the current
medial gastrocnemius fascicle length of healthy control study was relatively small, although significant differences in
changed from 28 to 78mm across the ankle and knee positions. biomechanical properties were still observed.
The results on medial gastrocnemius fascicle length normalized
to the lower-leg length also showed similar results. Arampatzis
et al26 reported a range from 37 to 67mm across 6 ankle and CONCLUSIONS
knee angle combinations with the ankle position between 20° The present study found that compared with healthy sub-
plantar flexion and 10° dorsiflexion. The larger range of fasci- jects, stroke survivors showed simultaneous changes at the
cle length in our study may arise from the larger range of ankle fascicle and joint levels, including decreased length and re-
and knee positions (ankle position between 45° plantar flexion duced pennation angle of the muscle fascicles, and decreased
and 15° dorsiflexion). Because of the lack of published data, ROM and increased stiffness in dorsiflexion at the joint. Bio-
direct comparisons could not be made for the results on stroke mechanic changes at the fascicle and joint levels were corre-
survivors. lated to each other, and the changes at the joint may originate
Muscle force is transmitted to the tendon at a pennation from the muscle fascicles. Clinical symptoms of spasticity/
angle with muscle force scaled according to the cosine of the contracture may be closely related to changes in muscle archi-
pennation angle.9,23,29 It has been reported that hypertrophy of tecture, including shortening of muscle fascicles and reduction
muscles involves an increase in pennation angle.9 In contrast, of pennation angle. In vivo evaluation of both muscle and joint

Arch Phys Med Rehabil Vol 90, May 2009


FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao 825

Fig 5. Anterior pennation an-


gles of both healthy subjects
(dark line) and stroke survi-
vors (gray line) at 4 knee posi-
tions: (A) full knee extension,
(B) 30° knee flexion, (C) 60°
knee flexion, and (D) 90° knee
flexion. * Significant differ-
ences between the 2 popula-
tions. P<.05 (t test). Abbrevia-
tions: DF, dorsiflexion; PF,
plantarflexion.

properties may serve as a quantitative tool in stroke rehabili- 8. Lieber RL, Bodine-Fowler SC. Skeletal muscle mechanics: impli-
tation and outcome evaluation. cations for rehabilitation. Phys Ther 1993;73:844-56.
9. Kawakami Y, Abe T, Fukunaga T. Muscle-fiber pennation angles
References are greater in hypertrophied than in normal muscles. J Appl
1. Singer B, Dunne J, Allison G. Reflex and non-reflex elements of
Physiol 1993;74:2740-4.
hypertonia in triceps surae muscles following acquired brain
injury: implications for rehabilitation. Disabil Rehabil 2001;23: 10. Maganaris CN, Baltzopoulos V, Sargeant AJ. In vivo mea-
749-57. surements of the triceps surae complex architecture in man:
2. Harlaar J, Becher JG, Snijders CJ, Lankhorst GJ. Passive stiffness implications for muscle function. J Physiol (Lond) 1998;512:
characteristics of ankle plantar flexors in hemiplegia. Clin Bio- 603-14.
mech (Bristol, Avon) 2000;15:261-70. 11. Magnusson SP, Aagaard P, Dyhre-Poulsen P, Kjaer M. Load-
3. Katz RT, Rymer WZ. Spastic hypertonia: mechanisms and mea- displacement properties of the human triceps surae aponeurosis in
surement. Arch Phys Med Rehabil 1989;70:144-55. vivo. J Physiol 2001;531:277-88.
4. Singer B, Dunne J, Singer KP, Allison G. Evaluation of triceps 12. Shortland AP, Harris CA, Gough M, Robinson RO. Architecture
surae muscle length and resistance to passive lengthening in of the medial gastrocnemius in children with spastic diplegia. Dev
patients with acquired brain injury. Clin Biomech (Bristol, Avon) Med Child Neurol 2001;43:796-801.
2002;17:152-61. 13. Cheatwood AP, Rethlefsen SA, Kay RM, Wren TA. Changes in
5. Vattanasilp W, Ada L, Crosbie J. Contribution of thixotropy, medial gastrocnemius architecture with spasticity and contracture.
spasticity, and contracture to ankle stiffness after stroke. J Neurol In: Proceedings of the 52nd Annual Meeting of the Orthopaedic
Neurosurg Psychiatry 2000;69:34-9. Research Society; Chicago; 2006.
6. Zhang LQ, Wang G, Nishida T, Xu D, Sliwa JA, Rymer WZ. 14. Li L, Tong KY, Hu X. The effect of poststroke impairments on
Hyperactive tendon reflexes in spastic multiple sclerosis: measures brachialis muscle architecture as measured by ultrasound. Arch
and mechanisms of action. Arch Phys Med Rehabil 2000;81:901-9. Phys Med Rehabil 2007;88:243-50.
7. Chung SG, van Rey EM, Bai Z, Roth EJ, Zhang L-Q. Biome- 15. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzo-
chanic changes in passive properties of hemiplegic ankles with poulos V, Maganaris CN. Differences in gastrocnemius muscle
spastic hypertonia. Arch Phys Med Rehabil 2004;85:1638-46. architecture between the paretic and non-paretic legs in children

Arch Phys Med Rehabil Vol 90, May 2009


826 FASCICLE- AND JOINT-LEVEL BIOMECHANICAL CHANGES IN STROKE, Gao

with hemiplegic cerebral palsy. Clin Biomech (Bristol, Avon) 27. Karamanidis K, Arampatzis A. Mechanical and morphological
2007;22:718-24. properties of different muscle-tendon units in the lower extremity
16. Mohagheghi AA, Khan T, Meadows TH, Giannikas K, Baltzo- and running mechanics: effect of aging and physical activity. J
poulos V, Maganaris CN. In vivo gastrocnemius muscle fascicle Exp Biol 2005;208:3907-23.
length in children with and without diplegic cerebral palsy. Dev 28. Maganaris CN. Force-length characteristics of the in vivo human
Med Child Neurol 2008;50:44-50. gastrocnemius muscle. Clin Anat 2003;16:215-23.
17. Fukashiro S, Hay DC, Yoshioka S, Nagano A. Simulation of 29. Gans C, de Vree F. Functional bases of fiber length and angulation
muscle-tendon complex during human movements. Int J Sport in muscle. J Morphol 1987;192:63-85.
Health Sci 2005;3:152-60. 30. Herring SW, Grimm AF, Grimm BR. Regulation of sarcomere
number in skeletal muscle: a comparison of hypotheses. Muscle
18. Bohannon RW, Smith MB. Interrater reliability of a modified
Nerve 1984;7:161-73.
Ashworth scale of muscle spasticity. Phys Therapy 1987;67:
31. Tabary JC, Tardieu C, Tardieu G, Tabary C, Gagnard L. Func-
206-7.
tional adaptation of sarcomere number of normal cat muscle.
19. Winter DA. Biomechanics and motor control of human move- J Physiol (Paris) 1976;72:277-91.
ment. 3rd ed. New York: John Wiley & Sons; 2004. 32. Williams PE, Goldspink G. Changes in sarcomere length and
20. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli physiological properties in immobilized muscle. J Anat 1978;127:
P. In vivo human gastrocnemius architecture with changing joint 459-68.
angle at rest and during graded isometric contraction. J Physiol 33. Friden J, Lieber RL. Spastic muscle cells are shorter and stiffer
1996;496:287-97. than normal cells. Muscle Nerve 2003;27:157-64.
21. Weng L, Tirumalai AP, Lowery CM, et al. US extended-field-of- 34. Svantesson U, Takahashi H, Carlsson U, Danielsson A, Sunner-
view imaging technology. Radiology 1997;203:877-80. hagen KS. Muscle and tendon stiffness in patients with upper
22. Kawakami Y, Kumagai K, Huijing PA, Hijakata T, Fukunaga T. motor neuron lesion following a stroke. Eur J Appl Physiol
The length-force characteristics of human gastrocnemius and so- 2000;82:275-9.
leus muscles in vivo. In: Herzog W, editor. Skeletal muscle 35. Friederich JA, Brand RA. Muscle fiber architecture in the human
mechanics: from mechanisms to function. Chichester: John Wiley lower limb. J Biomech 1990;23:91-5.
& Sons; 2000. p 327-41. 36. Wickiewicz TL, Roy RR, Powell PL, Edgerton VR. Muscle ar-
23. Fukunaga T, Roy RR, Shellock FG, et al. Physiological cross- chitecture of the human lower limb. Clin Orthop Relat Res 1983;
sectional area of human leg muscles based on magnetic resonance Oct(179):275-83.
imaging. J Orthop Res 1992;10:928-34. 37. Scott SH, Brown IE, Loeb GE. Mechanics of feline soleus, I:
24. Muraoka T, Chino K, Muramatsu T, Fukunaga T, Kanehisa H. In effect of fascicle length and velocity on force output. J Muscle Res
Cell Motil 1996;17:207-19.
vivo passive mechanical properties of the human gastrocnemius
38. Huijing PA. Architecture of the human gastrocnemius muscle and
muscle belly. J Biomech 2005;38:1213-9.
some functional consequences. Acta Anat (Basel) 1985;123:
25. Herbert RD, Moseley AM, Butler JE, Gandevia SC. Change in
101-7.
length of relaxed muscle fascicles and tendons with knee and
ankle movement in humans. J Physiol 2002;539:637-45. Suppliers
26. Arampatzis A, Karamanidis K, Stafilidis S, Morey-Klapsing G, a. JR3 Inc, 22 Harter Ave, Woodland, CA 95776.
DeMonte G, Bruggemann GP. Effect of different ankle- and b. GE LOGIQ-9, PO Box 414, Milwaukee, WI 53201.
knee-joint positions on gastrocnemius medialis fascicle length and c. MathWorks Inc, 3 Apple Hill Dr, Natick, MA 01730.
EMG activity during isometric plantar flexion. J Biomech 2006; d. MusculoGraphics Inc, 3617 Westwind Blvd, Santa Rosa, CA
39:1891-902. 95403.

Arch Phys Med Rehabil Vol 90, May 2009

You might also like