Beruflich Dokumente
Kultur Dokumente
www.elsevier.com/locate/clinbiomech
a,b,c,*
a
INSERM UMR S 731, 33 boulevard de Picpus, 75012 Paris, France
Universite Pierre et Marie Curie-Paris 6, 33 boulevard de Picpus, 75012 Paris, France
Service de Reeducation Neuro-orthopedique, Hopital Rothschild APHP, 33 boulevard de Picpus, 75012 Paris, France
b
Abstract
Background. Knee stability following an anterior cruciate ligament lesion has been widely studied. Only recent studies focused on the
contribution of the soleus muscle. Our purpose was to characterize the dynamic and muscular activity of balance recovery in healthy
subjects and patients with an anterior cruciate ligament rupture. The role of the soleus was investigated in the ipsilateral compensation
developed to stabilize the knee and in the contralateral compensation to recover balance.
Methods. Twelve anterior cruciate ligament decient patients, ten anterior cruciate ligament repaired patients and 14 control subjects
were recorded during a forward fall involving stepping to recover balance.
Findings. The dynamic of the centre of gravity remained normal when compared to the control group regardless of the treatment,
suggesting an adapted compensation to knee instability in this situation. A bilateral increase in soleus activity was related to an increased
duration in the balance recovery process in all patients. Patients used one of two strategies to recover balance regardless of the treatment:
reducing the step length, involving an early recruitment of the soleus before heel contact, or anticipating braking with a similar step
length requiring a predominant activity of the hamstrings.
Interpretations. These results suggest that bilateral activity of the soleus is involved to compensate for instability and highlight the
contribution of the soleus to rehabilitation after an anterior cruciate ligament lesion, not only as a compensatory muscle acting at
the knee level but also at a higher level in the bilateral control of stance.
2006 Elsevier Ltd. All rights reserved.
Keywords: Anterior cruciate ligament; Neuromuscular control; Soleus muscle; Balance recovery
1. Introduction
The control of postural balance depends on various systems (nervous system, locomotor apparatus). A lesion in
any of these can lead to a perturbation of postural reactions. In clinical practice, pathology may associate several
lesions that perturb the control of equilibrium. This is the
Corresponding author.
E-mail address: philippe.thoumie@rth.aphp.fr (P. Thoumie).
0268-0033/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.clinbiomech.2006.04.002
850
tion of the soleus could be associated with a dierent balance recovery strategy after an ACL lesion (repaired or
not), and that surgical restoration of the stability of the
knee should be associated with a modication of the strategy used by the ACLD subjects. Moreover, a bilateral
study of the soleus would also help distinguish between
the compensation directly linked to the lesion in ipsilateral
muscular activity and that of contralateral activity which
aims to control general balance.
2. Methods
2.1. Patients
Three groups of subjects took part in the study: a control group comprising 14 healthy subjects with no pathology of the knee, a group of 12 ACL decient knee patients
(ACLD) having an unilateral lesion of the ACL conrmed
clinically (Lachman test) and by magnetic resonance imaging, a group of 10 ACL knee surgically reconstructed
patients (ACLR) with an unilateral lesion of the ACL conrmed during surgery. Knee joint pain, eusion and limitation of the full knee joint range of motion were exclusion
criteria of the study.
Two of the patients were regular participant in high level
sport activities and surgically treated 2.5 months after the
lesion. All others were recreational sport participants, only
participating occasionally in sport activities like skiing and
jogging during holidays. They were surgically treated only
if they experienced instability of the knee during daily life
since their lesion. All reconstructed patients were treated
by the technique of Kenneth Jones except one reconstructed by the technique of Mac Intosh.
Most of the patients having a relatively poor level of
functional activities they were assessed before the test by
a questionnaire relevant to their capacities for walking,
going up and down stairs and jogging. At the time of the
test all patients armed to feel no discomfort in daily life
activities. Laxity of the knee joint was assessed clinically
and qualitatively by the same evaluator manually performing the Lachman test. All ACLD patients showed signicant drawer signs by comparison to ACLR subjects and
control group. The force of the quadriceps assessed by
the maximal voluntary isometric contraction manually
resisted (break test) and by squatting ability was considered
as normal.
The balance recovery test was performed at least three
months after the initial lesion (0.253 years) or surgical
treatment (0.453.5 years). A comparison of the time
elapsed between the test and the lesion or the surgery
(respectively 22(21) months in ACLD and 11(12) months
in ACLR) did not show statistical dierence with regard
to the treatment (Wilcoxon test, P = 0.34). All patients
underwent 6 weeks of rehabilitation programs from various physiotherapists in private practices or rehabilitation
centres. The three groups of subjects were homogeneous
in terms of height [1.73(0.1) m in CTL, 1.7(0.09) m in
851
852
rst according to the treatment. However, since no statistical dierence was found in the patient group with regard to
the treatment, the results were then compared for all combined patients.
3.1.1. Control group
The control subjects show a reproductive behaviour
identical to that previously described by Do et al. (1982).
Balance recovery includes rst a two-foot stance reaction
phase from release (t0) to toe-o (TO) with a duration of
263(SD: 24) ms. It is followed by a step execution phase
from toe-o to heel contact (HC) with a swing phase duration of 211(32) ms, with the contralateral foot remaining in
stance. Then the ground acceptance phase of the swinging
foot occurs, preceding execution of the second step.
Vertical biomechanical events of balance recovery rst
show (Fig. 2) a negative value of the vertical acceleration
of the CG (z00 G1), which corresponds to the fall of the
CG following the release of the restraining device. Then,
the reaction phase occurs corresponding to the reverse of
z00 G reaching a positive value (z00 G2) before toe-o. The
latency of z00 G2 is 187(15) ms and its amplitude is
3.17(1.03) m s2. Step execution begins with toe-o, ending
with foot contact of the swinging limb.
Fig. 2. Recordings of biomechanical parameters and EMG activities from the right and left soleus during a balance recovery step (right limb moving).
Single trial for a control subject: z00 G, z 0 G, zG are respectively the vertical acceleration, velocity and position of the centre of the gravity (U for upward)
z 0 Gmin is the negative peak of the vertical velocity and corresponds to the braking of the balance recovery (BP peak of braking speed), xP and yP the
antero-posterior and lateral displacement of the foot pressure (f for forward and s for stance, L for the length of the step), SOLm and SOLs, raw EMG
activity of the soleus from the moving and the stance limb.
853
Table 1
Mean values of the temporo-spatial components of the balance recovery step after a forward fall and the biomechanical parameters of the dynamic of the
centre of gravity per group with respect to the treatment (ACLD, ACLR) and respective P values
Parameters
ACLD
Swinging limb
Uninjured side
Injured side
Uninjured side
ACLR
Injured side
P value
665(50)
291(45)
234(24)
55(9)
0.99(0.33)
208(18)
3.27(0.88)
0.246(0.08)
0.004(0.018)
0.616(0.169)
657(53)
301(92)
234(25)
54(10)
0.98(0.25)
199(28)
3.46(1.05)
0.253(0.077)
0.003(0.014)
0.596(0.169)
654(64)
285(39)
245(24)
49(8)
0.93(0.29)
201(38)
2.60(0.75)
0.185(0.069)
0.001(0.016)
0.613(0.180)
672(81)
296(45)
245(31)
53(12)
0.92(0.30)
204(39)
2.62(1.09)
0.175(0.086)
0.000(0.023)
0.596(0.166)
NS
NS
NS
NS
NS
NS
NS
NS
NS
NS
Z00 G1: negative peak of the vertical acceleration of the centre of gravity (CG) before toe-o of the swing limb.
Z00 G2: positive peak of the vertical acceleration of the reaction phase (before toe-o).
Z 0 G at HC: vertical velocity of the CG at heel contact (end of the swing phase).
DZG at HC, variation of the height of the CG at heel contact.
Table 2
Mean values of the temporo-spatial components of the balance recovery step and the biomechanical parameters of the dynamic of the centre of gravity
after a forward fall, per group, with respect to the time of braking
Parameters
Control
Braking patients
Non-braking patients
Swinging limb
Normal
Uninjured side
Injured side
Uninjured side
Injured side
592(43)
263(24)
474(46)
211(32)
26(20)
57(9)
1.21(0.27)
187(15)
3.17(1.03)
0.225(0.07)
0.008(0.021)
0.754(0.068)
3.6(0.5)
667(41)**
290(43)
536(40)*
247(20)*
9(10)
51(8)
0.94(0.35)
209(32)
3.08(0.89)
0.241(0.057)
0(0.018)
0.686(0.135)
2.8(0.7)**
668(44)**
294(41)
536(57)*
242(26)*
16(17)**,
52(10)
0.87(0.29)
208(30)
3.20(1.13)
0.212(0.09)
0.001(0.016)
0.664(0.147)
2.8(0.6)**
654(67)**
289(34)
522(44)*
233(26)*
11(17)
54(9)
0.99(0.28)
202(34)
2.87(0.89)
0.199(0.093)
0.004(0.018)
0.555(0.18)**,
2.4(0.7)**
660(82)**
282(47)
519(58)*
236(30)*
20(17)
54(11)
1.02(0.24)
195(35)
2.98(1.16)
0.221(0.091)
0.004(0.02)
0.539(0.16)**,
2.3(0.6)**
db is the braking time (=tz 0 Gmin-tHC). Vs is the velocity of the step (=ratio of the length of the step to the swing phase duration).
P values: *P < 0.05, **P < 0.01, signicantly dierent from control; P < 0.05, P < 0.01, signicantly between subgroups.
854
Fig. 3. Recordings of some of the biomechanical parameters of the balance recovery step and some of the EMG activities for a control subject (CTL), an
ACL subject who brakes before heel contact (B) and an ACL subject who brakes after heel contact (NB). Single trial for each subject. The swinging limb
was the left leg for the CTL and the injured leg for the ACL. Vertical solid line shows the time of release (t0) and the dotted lines correspond to the time of
toe o (TO, start of the step execution phase) and heel contact (HC, end of the swing phase). z00 G and z 0 G are the vertical acceleration and velocity (U,
upward), L on xP graph is the length of the rst step executed to recover balance (F, forward and L, step length, BP peak of braking speed). SOLm and
HAMm are respectively the soleus and hamstrings muscle activities of the moving limb.
ery does not show any dierence between the ACLR and
ACLD subjects, EMG data were rst analysed with respect
to the treatment, then for the entire group.
3.2.1. Control group
On the moving limb, each muscle shows two bursts of
EMG (Figs. 3 and 4). The soleus is the rst muscle to
become active. Its activity starts 65(11) ms after the release
of the restraining device and ceases 189(31) ms after [duration 124(31) ms]. This burst occurs before the positive peak
of vertical acceleration of the CG and ends a short while
afterwards. This activity corresponds to the reaction to
the fall occurring just after release (Thoumie and Do,
1996). The second burst of the soleus appears after TO
[433(63) ms after the release] and occurs 63(43) ms before
heel contact, preparing to stabilize the swinging limb during
the ground acceptance phase, with the knee and ankle in
exion at the time of heel contact. The activity of the soleus
continues during the unilateral stance which follows.
The rst burst of the tibialis occurs 195(35) ms after
release and ends 333(42) ms afterwards with a 138(39) ms
mean duration, starting before TO and ending shortly
afterwards. It allows lifting the foot from the ground and
swinging. The second burst of the tibialis starts
435(47) ms after the release and occurs 64(29) ms before
HC. It prepares to stabilize the ankle at heel contact.
ms
Solm ipsi
Tam ipsi
Sols contra
ms
800
855
Tas contra
800
***
700
***
***
700
NS
600
600
HC 500
500
400
400
300
300
***
200
200
100
100
0
0
CTL
NB
CTL
ms
CTL
NB
NB
CTL
NB
-100
-100
Quam ipsi
800
HamMm ipsi
HamLm ipsi
***
***
700
**
NS
600
HC 500
400
300
200
100
0
CTL
NB
CTL
NB
CTL
NB
-100
Fig. 4. Mean values and standard deviations of EMG activities during balance recovery after a forward fall in control and patients regardless of the
treatment. EMG burst of the moving limb (injured side for the patient). From bottom to top: rst EMG burst duration, onset of the second EMG burst
and time of heel contact (HC). From left to right on the diagrams: control (CTL), braking (B) and non-braking (NB) groups. Right side of the gure
corresponds to the mean values of the moving limb, left side corresponds to that of the stance limb. HC is the time of heel contact, Solm, Tam, Quam,
HamM and HamL are respectively the Soleus, Tibialis, Quadriceps, Hamstrings medial and lateral muscle of the moving limb, IPSI correspond to the limb
ipsilateral to the lesion. Sols and Tas are the Soleus and Tibialis muscle of the stance limb, CONTRA corresponds to the limb contralateral to the lesion.
***P < 0.001, **P < 0.01.
The rst burst of the hamstrings medial (HamM) and lateral (HamL), respectively, lasts 114(51) ms and 127(40) ms.
It occurs respectively 70(12) ms and 78(25) ms after the
release and ends afterward [respectively 183(55) ms and
206(58) ms]. These bursts occur before the positive peak
of the vertical acceleration and end shortly afterwards. They
act again as a posterior muscular activity reacting to the forward fall. The second burst of these muscles occurs
378(63) ms and 411(69) ms, respectively, after the release
during the swing phase. These bursts start before HC
[116(39) ms for HamM and 89(41) ms for HamL] to control
the extension of the knee during the swing phase, and then
to stabilize the lower limb during the ground acceptance
phase while the hip and knee are in exion at the time of
heel contact. These muscular activities occur during the unilateral stance which follows.
Quadriceps shows a rst burst occurring 178(47) ms
after release and ending 336(37) ms afterward [duration
159(51) ms]. This burst occurs around TO, starting a little
before and ending afterward. This burst makes it possible
856
857
858
limb stiness when elderly subjects step down. They conclude that this is a strategy to compensate for their reduced
motor control capacities.
We observed an increase in the contralateral activity
duration of both recorded muscles in the uninjured limb.
This suggests that muscular activity of the stance limb
helps protect the injured knee during the weight acceptance
phase of the fall after swinging with the injured limb, by
slowing down the forward progression of the body, thereby
reducing the impact of ground acceptance. This hypothesis
is supported by the results of other authors (Michel and
Do, 2002) who concluded that the function of the soleus
is to control the forward body progression in balance
recovery and gait initiation.
In all ACL groups, preparation for the ground acceptance phase of the injured moving limb is characterized by
an increase in the time elapsed between the burst of hamstrings and heel contact. These results resemble the changes
in the hamstrings activity of ACL subjects (facilitation, timing of activation, duration, time of beginning and peak) previously reported in normal or ascent gait (Kalund et al.,
1990; Lass et al., 1991; Beard et al., 1994; Kvist and Gillquist, 2001; Rudolph et al., 2001; Boerboom et al., 2001).
In the patients (B and NB), the early activation of the hamstrings compared to HC would signicantly reduce the step
execution velocity in order to stabilize the knee at heel contact of the ground and thus to protect it. Early activation of
the hamstrings with respect to heel contact also suggests an
anticipation in the control of the forward translation of the
tibia attributed to these muscles when the knee is extended in
an open kinetic chain (Solomonow et al., 1987; Baratta et al.,
1988). The early activation of the hamstrings medial is characteristic of the strategy of the B group compared to the NB
group. Since patients of the B group are the only ones to
brake before heel contact, the hamstrings medial could play
a prevalent role in anticipating the stabilization of the knee
at heel contact for this group. This hypothesis can be related
to that of Alkjaer et al. (2002) who showed that activity of
the hamstrings medial (semi tendinosus) was greater as the
knee extends in a forward lunge in ACLD coper subjects
compared with non-copers and with the control.
The early activation of the second burst of the soleus is
characteristic primarily of the behaviour of the ACLD and
NB groups. It does not seem to be related solely to the passive mechanical instability of the knee since there is the
same number of ACLD and ACLR subjects in the NB
group and that the respective time of activation of the
soleus does not dier in these two subgroups. Various
authors (Sutherland et al., 1980; Ciccotti et al., 1994) have
highlighted the role of the soleus in stabilizing the knee
during the unilateral stance phase of gait and Ciccotti
et al. (1994) reports that the activity of the soleus is
increased at this phase in ACLD subjects.
Recent studies (Elias et al., 2003; Sherbondy et al., 2003)
reported that the soleus (solicited in a mock closed kinetic
chain situation) could act as an agonist of the ACL by pulling backwards the proximal part of the tibia. This action of
Acknowledgment
We thank Ms K. De Haan for reviewing the English in
this article.
References
Adachi, N., Ochi, M., Uchio, Y., Iwasa, J., Ryoke, K., Kuriwaka, M.,
2002. Mechanoreceptors in the anterior cruciate ligament contribute to
the joint position sense. Acta Orthop. Scand. 73, 330334.
Alkjaer, T., Simonsen, E.B., Peter Magnusson, S.P., Aagaard, H.,
Dyhre-Poulsen, P., 2002. Dierences in the movement pattern of a
forward lunge in two types of anterior cruciate ligament decient
patients: copers and non-copers. Clin. Biomech. (Bristol, Avon) 17,
586593.
Alkjaer, T., Simonsen, E.B., Jorgensen, U., Dyhre-Poulsen, P., 2003.
Evaluation of the walking pattern in two types of patients with
anterior cruciate ligament deciency: copers and non-copers. Eur. J.
Appl. Physiol. 89, 301308.
Baratta, R., Solomonow, M., Zhou, B.H., Letson, D., Chuinard, R.,
DAmbrosia, R., 1988. Muscular coactivation. The role of the
antagonist musculature in maintaining knee stability. Am. J. Sports
Med. 16, 113122.
Beard, D.J., Dodd, C.A., Trundle, H.R., Simpson, A.H., 1994. Proprioception enhancement for anterior cruciate ligament deciency. A
prospective randomised trial of two physiotherapy regimes. J. Bone
Joint Surg. Br. 76, 654659.
Beard, D., Soundarapandian, R., OConnor, J., Dodd, C.A.F., 1996. Gait
and electromyographic analysis of anterior cruciate ligament decient
subjects. Gait Posture, 8388.
Berchuck, M., Andriacchi, T.P., Bach, B.R., Reider, B., 1990. Gait
adaptations by patients who have a decient anterior cruciate
ligament. J. Bone Joint Surg. Am. 72, 871877.
Boerboom, A.L., Hof, A.L., Halbertsma, J.P., van Raaij, J.J., Schenk, W.,
Diercks, R.L., van Horn, J.R., 2001. Atypical hamstrings electromyographic activity as a compensatory mechanism in anterior cruciate
ligament deciency. Knee Surg. Sports Traumatol. Arthrosc. 9, 211
216.
Bonm, T.R., Jansen Paccola, C.A., Barela, J.A., 2003. Proprioceptive
and behavior impairments in individuals with anterior cruciate
ligament reconstructed knees. Arch. Phys. Med. Rehabil. 84, 1217
1223.
Chmielewski, T.L., Rudolph, K.S., Snyder-Mackler, L., 2002. Development of dynamic knee stability after acute ACL injury. J. Electromyogr. Kinesiol. 12, 267274.
Ciccotti, M.G., Kerlan, R.K., Perry, J., Pink, M., 1994. An electromyographic analysis of the knee during functional activities. II. The
anterior cruciate ligament-decient and -reconstructed proles. Am. J.
Sports Med. 22, 651658.
Corrigan, J.P., Cashman, W.F., Brady, M.P., 1992. Proprioception in the
cruciate decient knee. J. Bone Joint Surg. Br. 74, 247250.
Do, M.C., Breniere, Y., Brenguier, P., 1982. A biomechanical study
of balance recovery during the fall forward. J. Biomech. 15,
933939.
Do, M.C., Schneider, C., Chong, R.K., 1999. Factors inuencing the
quick onset of stepping following postural perturbation. J. Biomech.
32, 795802.
Elias, J.J., Faust, A.F., Chu, Y.H., Chao, E.Y., Cosgarea, A.J., 2003. The
soleus muscle acts as an agonist for the anterior cruciate ligament. An
in vitro experimental study. Am. J. Sports Med. 31, 241246.
Hortobagyi, T., DeVita, P., 2000. Muscle pre- and coactivity during
downward stepping are associated with leg stiness in aging.
J. Electromyogr. Kinesiol. 10, 117126.
859
Iwasa, J., Ochi, M., Adachi, N., Tobita, M., Katsube, K., Uchio, Y., 2000.
Proprioceptive improvement in knees with anterior cruciate ligament
reconstruction. Clin. Orthop., 168176.
Johansson, H., Sjolander, P., Sojka, P., 1991. Receptors in the knee joint
ligaments and their role in the biomechanics of the joint. Crit. Rev.
Biomed. Eng. 18, 341368.
Kalund, S., Sinkjaer, T., Arendt-Nielsen, L., Simonsen, O., 1990. Altered
timing of hamstring muscle action in anterior cruciate ligament
decient patients. Am. J. Sports Med. 18, 245248.
Kvist, J., 2004. Sagittal plane translation during level walking in poorfunctioning and well-functioning patients with anterior cruciate
ligament deciency. Am. J. Sports Med. 32, 12501255.
Kvist, J., Gillquist, J., 2001. Anterior positioning of tibia during motion
after anterior cruciate ligament injury. Med. Sci. Sports Exerc. 33,
10631072.
Lass, P., Kaalund, S., leFevre, S., Arendt-Nielsen, L., Sinkjaer, T.,
Simonsen, O., 1991. Muscle coordination following rupture of the
anterior cruciate ligament. Electromyographic studies of 14 patients.
Acta Orthop. Scand. 62, 914.
Lewek, M.D., Chmielewski, T.L., Risberg, M.A., Snyder-Mackler, L.,
2003. Dynamic knee stability after anterior cruciate ligament rupture.
Exerc. Sport Sci. Rev. 31, 195200.
Lysholm, M., Ledin, T., Odkvist, L.M., Good, L., 1998. Postural
controla comparison between patients with chronic anterior cruciate
ligament insuciency and healthy individuals. Scand. J. Med. Sci.
Sports 8, 432438.
Michel, V., Do, M.C., 2002. Are stance ankle plantar exor muscles
necessary to generate propulsive force during human gait initiation?
Neurosci. Lett. 325, 139143.
Noyes, F.R., Mooar, P.A., Matthews, D.S., Butler, D.L., 1983. The
symptomatic anterior cruciate-decient knee. Part I: The long-term
functional disability in athletically active individuals. J. Bone Joint
Surg. Am. 65, 154162.
Rudolph, K.S., Snyder-Mackler, L., 2004. Eect of dynamic stability on a
step task in ACL decient individuals. J. Electromyogr. Kinesiol. 14,
565575.
Rudolph, K.S., Axe, M.J., Buchanan, T.S., Scholz, J.P., Snyder-Mackler,
L., 2001. Dynamic stability in the anterior cruciate ligament decient
knee. Knee Surg. Sports Traumatol. Arthrosc. 9, 6271.
Sherbondy, P.S., Queale, W.S., McFarland, E.G., Mizuno, Y., Cosgarea,
A.J., 2003. Soleus and gastrocnemius muscle loading decreases
anterior tibial translation in anterior cruciate ligament intact and
decient knees. J. Knee Surg. 16, 152158.
Snyder-Mackler, L., Fitzgerald, G.K., Bartolozzi 3rd., A.R., Ciccotti,
M.G., 1997. The relationship between passive joint laxity and
functional outcome after anterior cruciate ligament injury. Am. J.
Sports Med. 25, 191195.
Solomonow, M., Baratta, R., Zhou, B.H., Shoji, H., Bose, W., Beck, C.,
DAmbrosia, R., 1987. The synergistic action of the anterior cruciate
ligament and thigh muscles in maintaining joint stability. Am. J. Sports
Med. 15, 207213.
Sutherland, D.H., Cooper, L., Daniel, D., 1980. The role of the ankle
plantar exors in normal walking. J. Bone Joint Surg. Am. 62,
354363.
Thoumie, P., Do, M.C., 1996. Changes in motor activity and biomechanics during balance recovery following cutaneous and muscular
deaerentation. Exp. Brain Res. 110, 289297.
Torry, M.R., Decker, M.J., Ellis, H.B., Shelburne, K.B., Sterett, W.I.,
Steadman, J.R., 2004. Mechanisms of compensating for anterior
cruciate ligament deciency during gait. Med. Sci. Sports Exerc. 36,
140314012.
Williams, G.N., Barrance, P.J., Snyder-Mackler, L., Buchanan, T.S.,
2004. Altered quadriceps control in people with anterior cruciate
ligament deciency. Med. Sci. Sports Exerc. 36, 10891097.