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THE AMERICAN JOURNAL OF SPORTS MEDICINE, Vol. 31, No. 2
© 2003 American Orthopaedic Society for Sports Medicine

The Soleus Muscle Acts as an Agonist for


the Anterior Cruciate Ligament
An In Vitro Experimental Study
John J. Elias, PhD, Alfred F. Faust, MD, Yung-Hua Chu, MS, Edmund Y. Chao, PhD,
and Andrew J. Cosgarea,* MD

From the Department of Orthopaedic Surgery and the Orthopaedic Biomechanics Laboratory,
Johns Hopkins University, Baltimore, Maryland

Background: Although the quadriceps muscles are known antagonists for the anterior cruciate ligament and the hamstring
muscles are known agonists, the influence of the calf muscles on knee stability is not well understood.
Hypothesis: The soleus muscle acts as an anterior cruciate ligament agonist and the gastrocnemius muscle acts as an anterior
cruciate ligament antagonist.
Study Design: Controlled laboratory study.
Methods: Six cadaveric knees were tested with individual and combined activation of the gastrocnemius and soleus muscles
to determine the influence of simulated muscle contraction on tibiofemoral motion.
Results: At all flexion angles, applying the soleus muscle force tended to translate the tibia posteriorly, whereas applying the
gastrocnemius muscle force tended to translate the tibia anteriorly. Applying the soleus and gastrocnemius muscle forces
together also tended to translate the tibia anteriorly. The average anterior and posterior tibial translations were greatest at 50°
of flexion.
Conclusions: The soleus muscle is capable of acting as an agonist for the anterior cruciate ligament and the gastrocnemius
muscle can act as an antagonist.
Clinical Relevance: A better understanding of the agonistic behavior of the soleus muscle on the anterior cruciate ligament may
lead to the development of training and rehabilitation strategies that could reduce the incidence of injury and improve function
in both patients with anterior cruciate ligament deficiency and patients who have undergone anterior cruciate ligament
reconstruction.
© 2003 American Orthopaedic Society for Sports Medicine

The ACL is the primary passive restraint against patho- The calf muscles are active during activities that put the
logic anterior tibial translation. Muscles that dynamically ACL at risk of rupture, such as cutting movements and
resist anterior tibial translation act as ACL agonists, landing from a jump.13 However, investigators have
whereas muscles that dynamically produce anterior tibial mainly focused on the influence of these muscles on ankle
translation act as ACL antagonists. Because the ham- stability.4, 20, 23 The calf muscles, the soleus muscle, and
string muscles attach on the proximal tibia and exert a the medial and lateral heads of the gastrocnemius muscle,
force with a posterior orientation when the knee is flexed, in particular, plantar flex the foot and can decelerate the
they are considered the primary ACL agonists.16, 18, 22 rotation of the tibia around the ankle to modulate ankle
Conversely, the quadriceps muscles are considered ACL dorsiflexion when the foot is planted. Because the heads of
antagonists.5, 22 the gastrocnemius muscle originate on the distal femur
and insert on the posterior calcaneus, thereby crossing the
knee joint, their role in knee stabilization has been inves-
tigated. Theoretical21 and in vivo experimental9 studies
* Address correspondence and reprint requests to Andrew J. Cosgarea, have indicated that the gastrocnemius muscle acts as an
MD, Orthopaedic Surgery, Johns Hopkins Sports Medicine, 10753 Falls Road, antagonist for the ACL, although another in vitro experi-
Suite 215, Baltimore, MD 21093.
No author or related institution has received any financial benefit from mental study indicated that activation of the gastrocne-
research in this study. See “Acknowledgment” for funding information. mius muscle strains the PCL, rather than the ACL.5

241
242 Elias et al. American Journal of Sports Medicine

Because the soleus muscle does not cross the knee joint,
the possible influence of soleus muscle loading on ACL
strain has generally been ignored. Unlike the gastrocne-
mius muscle, the soleus muscle originates on the proximal
tibia. With the foot planted, the force exerted by the soleus
muscle that resists forward rotation of the tibia about the
ankle could theoretically limit anterior translation of the
proximal tibia with respect to the distal femur. To the best
of our knowledge, no other investigators have explored the
role of the soleus muscle in stabilizing the knee joint. For
the current study, we hypothesized that the soleus and
gastrocnemius muscles have opposite influences on tibial
translation. We believe that activation of the gastrocne-
mius muscle tends to translate the tibia anteriorly,
thereby loading the ACL, whereas activation of the soleus
muscle tends to translate the tibia posteriorly, thereby
unloading the ACL. In vitro kinematic testing was per-
formed to investigate the proposed hypothesis.

MATERIALS AND METHODS


Six knees harvested from six cadavers with ages ranging
from 67 to 77 years were used for kinematic testing. The
knees were free of deformities and showed no signs of
prior surgeries. Each knee was dissected to isolate the
quadriceps tendon, the semimembranosus tendon, and the
biceps femoris tendon. The gastrocnemius and soleus
muscles were completely separated from one another, in-
Figure 1. Each knee was positioned at 20°, 50° and 80° of
cluding distally where the tendinous contributions to the
flexion with loads applied to simulate quadriceps (quads) and
Achilles tendon were carefully dissected apart. All other
hamstring (hams) muscle forces. The gastrocnemius (gas-
muscles were removed, without disrupting the joint cap-
trocs) and soleus muscle were loaded individually and in
sule, patellar retinaculum, or patellofemoral ligaments.
combination by using constant force springs. Each knee was
Before testing, each knee was aligned by using a standard-
tested with the ACL intact and with the ACL cut and with and
ized radiographic technique described previously17 to pro-
without application of an anterior load.
duce a neutral varus-valgus orientation and internal-ex-
ternal rotation at 0° of flexion. Electromagnetic sensors
(Flock of Birds, Ascension Technology, Burlington, Ver- actuator through a linkage that divided the actuator load
mont) were secured to the femur, tibia, and patella to equally between the two tendons. The gastrocnemius and
quantify the kinematics of the knee. The tibiofemoral ro- soleus muscles were each loaded using a 180-N constant
tations were quantified with a standardized knee coordi- force spring. The springs were secured to a frame fixed to
nate system11 established during the alignment process. the materials testing platform. The gastrocnemius and
Tibial translations were expressed with respect to a local soleus muscles were wrapped around low friction rollers
coordinate system fixed to the femur at the intersection of also fixed to the platform. The rollers were positioned to
the knee screw axis and a sagittal plane bisecting the reproduce the anatomic orientation of the gastrocnemius
knee. The knee screw axis was established between 0° and and soleus muscles with respect to the tibia. To load the
90° of flexion. Each translation and rotation was set to gastrocnemius and soleus muscles, we extended the
zero at full extension. springs and secured them to the muscles by using No. 5
The cadaveric knees were used to characterize the in- braided nonabsorbable suture sewn into the tendon with
fluence of simulated muscle activation of the soleus and an interlocking stitch. The spring force was independent
gastrocnemius muscles on the motion of the tibia. A knee of the spring extension because of the constant force
simulator6, 18, 19 was used to control the quadriceps and spring design, ensuring that each muscle carried a load of
hamstring muscle forces and hip loads applied to the knee 180 N.
at various flexion angles (Fig. 1). The hip load was applied Before testing at each prescribed flexion angle, each
through the main actuator of a modified Bionix 858 ma- knee was placed in its neutral position, based on the
terials testing platform (MTS, Eden Prairie, Minnesota). anatomic coordinate system. A 100-N load was applied to
Two additional independent actuators applied the ham- the quadriceps and hamstring muscles, and the knee was
string and quadriceps muscle loads through a cable and flexed to the appropriate angle. At 20° and 50° of flexion,
pulley system. A cryoclamp device secured the quadriceps a 180-N force was applied to the hamstring muscles while
tendon to one actuator. Two other cryoclamps secured the a 540-N force was applied to the quadriceps muscles. At
semimembranosus and biceps femoris tendons to a second 80° of flexion, a 180-N force was applied to the hamstring
Vol. 31, No. 2, 2003 The Soleus Muscle as ACL Agonist 243

muscles while a 720-N force was applied to the quadriceps but before the soleus and gastrocnemius muscles were
muscles. The hip load was varied to hold the knee at the loaded, the tibia was significantly less anterior when the
prescribed flexion angle but was approximately equal to ACL was intact and no anterior load was applied (test case
120 N for all tests. The hamstring muscle force was set to 1) than for any of the three other test cases (Fig. 2). Also,
180 N on the basis of previous theoretical calculations at these flexion angles, the tibia was significantly more
showing that the peak gastrocnemius muscle force is ap- anterior when the ACL was cut and an anterior load was
proximately equal to the peak hamstring muscle force for applied (test case 4) than for any of the three other test
multiple functional activities.12, 15 The quadriceps muscle cases. At 50° of flexion, the variation between test cases
force at each flexion angle was based on a previously was not statistically significant (P ⫽ 0.13). The average
measured ratio of the quadriceps muscle force to the ham- anterior shift from test case 1 to test case 4 was approxi-
string muscle force for the knee simulator during simu- mately 6 mm at 20° of flexion, 1.5 mm at 50° of flexion, and
lated closed chain knee extension. With the knee at each less than 1 mm at 80° of flexion. The test case did not
fixed flexion angle (20°, 50°, and 80°) and the quadriceps significantly influence the original varus/valgus orienta-
and hamstring muscle forces applied, the gastrocnemius tion, internal/external rotation, or medial/lateral shift of
and soleus muscles were loaded individually and in com- the tibia at any flexion angle.
bination to simulate activation of these muscles, while the When the soleus muscle force was applied, the tibia
motion of the tibia in response to each load was quantified. translated posteriorly with respect to the femur. At 20° of
Each knee was initially tested in the intact state (test flexion (Fig. 3A), the measured tibial shifts caused by
case 1). The gastrocnemius and soleus muscle forces were application of soleus or gastrocnemius muscle forces, or
also applied after applying an additional 110-N force to both, were not significant for any of the four test cases
translate the tibia anteriorly (test case 2). The anterior (0.06 ⬍ P ⬍ 0.20). The posterior tibial shift that occurred
force was applied in the anterior-posterior plane, perpen- after application of a load through the soleus tendon was
dicular to the long axis of the tibia, by using a suspended statistically significant for all four test cases at 50° of
weight and a cable and pulley system. An S-hook on the flexion (Fig. 3B). For the four test cases, the average
end of the cable was hooked to a plastic U-bolt attached to posterior shift of the tibia occurring in response to loading
a Kirschner wire that passed through the proximal tibia. the soleus muscle ranged from 0.24 ⫾ 0.06 mm to 0.36 ⫾
The whole set of tests was performed for each knee with 0.07 mm. At 80° of flexion (Fig. 3C), the posterior shift was
the ACL intact and after sectioning the ACL (no anterior statistically significant only for test case 2 (P ⬍ 0.09 for
load, test case 3; anterior load, test case 4). The ACL was test case 3, P ⬍ 0.06 for test case 4).
sectioned through a 6-cm medial parapatellar approach. When the gastrocnemius muscle force was applied, the
The incision was closed with No. 2 braided nonabsorbable tibia translated anteriorly with respect to the femur. Al-
suture in an interrupted figure-of-eight fashion. After though no statistically significant changes were measured
testing was complete, we performed a second arthrotomy at 20° of flexion, the anterior shift of the tibia after appli-
on each specimen to confirm that the ACL had been com- cation of a load through the gastrocnemius tendon was
pletely sectioned.
For each combination of test case and flexion angle,
statistical comparisons were performed to determine the
influence of application of the gastrocnemius and soleus
muscle loads on the position of the tibia. A Friedman test
for nonparametric comparison of multiple groups with
repeated measures was used to determine whether appli-
cation of the gastrocnemius or soleus muscle load, or both,
significantly (P ⬍ 0.05) influenced the position of the tibia.
A nonparametric form of the Student-Neuman-Keuls test
was used for post hoc comparisons. Because of missing
data, only five knees were considered in statistical com-
parisons for the ACL-intact knees with no anterior load at
50° of flexion and for the ACL-deficient knees with an
anterior load at 80° of flexion. The same statistical tests
were also used to determine whether applying the ante-
rior load or cutting the ACL influenced the initial position
of the tibia before loading of the gastrocnemius and soleus
muscles.

RESULTS
Figure 2. The average anterior position of the tibia with
As expected, applying the anterior load and cutting the respect to the femur for the four test cases and the three
ACL caused the tibia to translate anteriorly with respect flexion angles before loading the soleus and gastrocnemius
to the femur. At both 20° and 80° of flexion, with quadri- muscles. The error bars represent the standard error of the
ceps and hamstring muscle co-contraction force applied mean.
244 Elias et al. American Journal of Sports Medicine

Applying the soleus and gastrocnemius muscle forces


together tended to translate the tibia anteriorly with re-
spect to the femur. The anterior shift of the tibia in re-
sponse to application of a combined gastrocnemius and
soleus muscle load was statistically significant for all test
cases except case 1 at 50° of flexion (P ⬍ 0.07) and was
statistically significant for all test cases at 80° of flexion.
Application of the calf muscle loads did not significantly
influence the varus/valgus orientation, the internal/exter-
nal rotation, or the medial/lateral shift of the tibia at any
flexion angle for any test case.

DISCUSSION
For this in vitro study, the soleus muscle acted as an ACL
agonist, whereas the gastrocnemius muscle acted as an
ACL antagonist. To our knowledge, no other study has
shown that the soleus muscle can act as an ACL agonist.
A previous in vivo study, in which ACL strain was meas-
ured while different muscles were activated, showed that
the gastrocnemius muscle acts as an ACL antagonist.9
The anterior translations produced by applying a gastroc-
nemius muscle force in this study would cause a smaller
increase in ACL strain than that seen in the in vivo
study.7, 8 This difference is most likely caused by differ-
ences in the loading conditions. The forces applied
through the quadriceps muscles, which are also ACL an-
tagonists, were larger for this in vitro study than for the
previous in vivo study. In addition, this in vitro study
modeled a simulated closed kinetic chain squat with co-
contraction of the quadriceps and hamstring muscles,
whereas the in vivo study was performed with the knee in
a nonweightbearing position. Joint loading from co-con-
traction and weightbearing increases joint stiffness and
decreases ACL strain.8
One unexpected finding of this study was that combined
loading of the soleus and gastrocnemius muscle produced
tibial translations similar to those seen after loading the
gastrocnemius muscle alone. The explanation of this phe-
nomenon is not clear from our data. We do believe, how-
ever, that this model probably oversimplifies the forces
acting on the lower leg. We applied a constant 180-N force
Figure 3. The average (⫾standard error) tibial anterior shift to both the gastrocnemius and soleus muscle at all flexion
caused by applying a 180-N force to the soleus and gastroc- angles. The literature suggests that even in full extension
nemius muscles individually and in combination at 20° (A), the soleus muscle probably exerts a greater plantar flex-
50° (B), and 80° (C) of knee flexion. Each knee was tested ion force than the gastrocnemius muscle.2, 3, 10 With in-
with the ACL intact and no anterior load (test case 1), with the creasing knee flexion, the length of the gastrocnemius
ACL intact and a 110-N anterior load (test case 2), with the muscle, which crosses both the knee and ankle joints,
ACL cut and no anterior load (3), and with the ACL cut and a decreases as the distance from the origins on the distal
110-N anterior load (4). A star indicates a statistically signif- femur to the insertion on the posterior calcaneus de-
icant anterior or posterior shift (P ⬍ 0.05). creases. In contrast, knee flexion does not change the
length of the soleus muscle, which crosses only the ankle
significant for all test cases except case 3 at 50° of flexion joint. Change in muscle length affects the capacity of the
(P ⬍ 0.06). At 50° of flexion, the largest anterior shift of muscle to generate contractile force. This phenomenon
the tibia in response to a gastrocnemius muscle load was results in a decreased ability of the gastrocnemius muscle
0.5 ⫾ 0.1 mm, for test case 1. In general, the anterior shift to generate force with increasing knee flexion angles in
of the tibia in response to a gastrocnemius muscle load comparison with the soleus muscle.2, 3, 10 Although it may
was slightly smaller at 80° of flexion than at 50° of flexion, have been more accurate for us to use a soleus muscle
but the shift was still statistically significant for all four force that was greater than the gastrocnemius muscle
test cases at 80° of flexion. force, we chose to use equal forces in our simplified model
Vol. 31, No. 2, 2003 The Soleus Muscle as ACL Agonist 245

because the actual soleus to gastrocnemius muscle force the situation of testing cadaveric tissue on a hydraulically
ratio has not been well defined, and we wanted to test our controlled knee simulator. In this study, the knees were
hypothesis using a worst-case scenario. The possibility tested at individual knee flexion angles, with relatively
exists that a greater soleus to gastrocnemius muscle force large quadriceps muscle loads with respect to the ham-
ratio would have decreased anterior tibial translation or string, soleus, and gastrocnemius muscle loads. Theoreti-
even translated the tibia posteriorly. Further study of the cal modeling has shown that the ratio of the quadriceps to
specific behavior of the calf muscles during sports activity hamstring muscle force can be greater than 2:1 during
is clearly warranted. normal gait1 and can exceed 8:1 during a seated knee
The tibial translations caused by gastrocnemius and so- extension exercise,15 whereas the peak force exerted by
leus muscle loading varied with the flexion angle. The ante- the hamstring and gastrocnemius muscles are simi-
rior translations were smallest at 20° of flexion. A possible lar.12, 15 For the current study, the ratio of the quadriceps
contributor to the decreased tibial anterior translation in to hamstring muscle force ranged from 3:1 at 20° of flexion
response to gastrocnemius muscle loading at 20° of flexion is to 4:1 at 80° of flexion, based on previous weightbearing
the original anterior position of the tibia with respect to the knee extension measurements made with the knee simu-
femur. For these in vitro test conditions, the initial anterior lator. The quadriceps muscle force was increased as the
position of the tibia was greatest at 20° of flexion. Therefore, static flexion angle increased to approximate in vivo load-
tensioning the gastrocnemius muscle may not have applied ing conditions. The magnitude of the hamstring muscle
pressure to the proximal tibia, which may be the mechanism force was equal to the magnitude of the gastrocnemius
by which the gastrocnemius muscle affects anterior tibial and soleus muscle forces. Because the quadriceps muscle
translation. The largest tibial translations were seen at 50° force has an anterior component acting on the tibia, de-
of flexion. The decrease in the tibial translations from 50° to creasing the ratio of the quadriceps muscle force to the
80° of flexion may be related to the increase in the quadri- soleus muscle force may have increased the ability of the
ceps muscle force. Additionally, the hamstring muscles be- soleus muscle to translate the tibia posteriorly. A large
come relatively more important as the direction of force quadriceps to soleus muscle force ratio was used for this
becomes more posterior with increasing knee flexion. Both of study, however, to provide a rigorous test of the proposed
these factors act together to increase joint stiffness, which hypothesis.
may have limited the ability of the soleus and gastrocnemius The results of this study suggest that the soleus muscle
muscles to translate the tibia with respect to the femur. The can potentially act as an ACL agonist, protecting it during
in vivo forces during sports activities or even during just dynamic activities. Even though the soleus muscle does
simple squatting are not well understood. Determination of not cross the knee joint, soleus muscle loading can produce
these forces would provide valuable information and lead to a moment that rotates the tibia with respect to the ankle,
a better understanding of dynamic stabilization. thereby shifting the proximal tibia posteriorly at the knee
Although four test cases with different combinations of joint. For static testing at individual flexion angles with
anterior load and ACL status were studied, the test case simulated quadriceps and hamstring muscle co-contrac-
had little influence on the relationship between calf mus- tion, simulated activation of the soleus and gastrocnemius
cle loading and tibial translations. Sectioning the ACL muscles produced relatively small tibial shifts. During
and applying an anterior load caused the tibia to be more dynamic activities, these muscles may have a greater in-
anterior before loading of the gastrocnemius and soleus fluence on ACL strain, however. The muscle forces and
muscles, particularly at 20° of flexion. The anterior shift external forces applied to the tibia were dramatically
caused by applying an anterior load and sectioning the smaller than what would be expected in vivo for activities
ACL decreased from 20° to 80° of flexion, most likely such as landing or pivoting, because of the loading limi-
because of the direction of the applied hamstring muscle tations of the knee simulator and the cadaveric tissue. The
force. The hamstring muscle force becomes more posterior goal of the current study was to show the direction of tibial
as the flexion angle increases and is therefore better able translation in response to the application of gastrocne-
to resist tibial anterior translation.16, 18, 22 Even though mius and soleus muscle forces, with the understanding
the test case had the greatest influence on the initial that the translation magnitude could increase for in vivo
position of the tibia at 20° of flexion, the test case did not load levels.
influence the statistical significance of the results at 20° of The muscle firing pattern and the loading rate of each
flexion. The flexion angle was a more important factor in muscle are important parameters governing tibiofemoral
determining the statistical significance of the tibial trans- kinematics. The results of this study indicate that simul-
lations than the test case. The similarity of the results for taneous activation of both calf muscles translates the tibia
the four test cases indicates that if these results hold true anteriorly, but that individual activation of the soleus
in vivo, the soleus muscle can potentially limit pathologic muscle could decrease tibial anterior translation. Because
tibial translation for an ACL-intact or ACL-deficient knee. a previous study showed that the soleus muscle tends to
In vivo, an ACL injury is most likely to occur when fire before the gastrocnemius muscle during cutting and
someone is landing from a jump or performing a quick stop pivoting activities,20 we believe that early activation of the
or a pivot.13 The ACL typically tears with the knee flexed, soleus muscle during dynamic activities could be a mech-
as the quadriceps muscles fire to decelerate knee flexion. anism acting to protect the ACL. This might be particu-
The large accelerations that occur and the large muscle larly important in female athletes, who have been shown
forces that are applied to the knee cannot be reproduced in to take longer to generate maximum hamstring muscle
246 Elias et al. American Journal of Sports Medicine

torque during isokinetic testing.14 Additionally, a better 7. Fleming BC, Beynnon BD, Nichols CE, et al: An in vivo comparison of
anterior tibial translation and strain in the anteromedial band of the ante-
understanding of the relative contributions of the gastroc- rior cruciate ligament. J Biomech 26: 51–58, 1993
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163–170, 2001
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forces using inverse dynamic optimization during flexion/extension of the
Funding for this work was provided by an Institutional knee. J Biomech Eng 121: 316 –322, 1999
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Research Grant from Johns Hopkins University. hamstring muscle loading on knee kinematics and in-situ forces in the
ACL. J Biomech 32: 395– 400, 1999
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