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Gait & Posture 28 (2008) 150–156


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Effects of plantarflexion on pelvis and lower limb kinematics


R. Brunner a,*, T. Dreher c, J. Romkes b, C. Frigo d
a
Neuro-Orthopaedic Department, University Children’s Hospital, Roemergasse 8, 4058 Basel, Switzerland
b
Laboratory for Movement Analysis, University Children’s Hospital, Basel, Switzerland
c
Department of Orthopaedic Surgery, Heidelberg, Germany
d
Department of Bioengineering, Politecnico, Milano, Italy
Received 15 April 2007; received in revised form 4 November 2007; accepted 18 November 2007

Abstract

Modelling the effect of soleus and gastrocnemius contractions against the floor resistance in a forward dynamics simulation revealed that
hip flexion, internal rotation and adduction together with external pelvic rotation could be attributed to a direct, but distant effect of triceps
surae contraction. Knee flexion smoothed out the effect. To validate this clinically relevant biomechanical observation, ankle plantar flexion
was correlated with hip and pelvic rotation retrospectively in children with spastic cerebral palsy.
In 49 children with spastic hemiplegia, plantar flexion showed a significant correlation with increased pelvic retraction and hip internal
rotation. In contrast, in 47 children with spastic diplegia no significant effect of the triceps surae on hip and pelvis kinematics was found.
Bilateral hip and knee flexion in diplegia appeared to prevent the proximal effect of the triceps surae seen in the hemiplegics. In diplegia
triceps surae overactivity did not appear to be a significant cause of internal rotation gait.
# 2007 Elsevier B.V. All rights reserved.

Keywords: Soleus gastrocnemius function; Biomechanical modelling; Hip internal rotation; Pelvic retraction; Spastic plantarflexion

1. Introduction remained inconclusive [8]. Delp et al. suggested possible


mechanisms, such as hip flexion deformity that increases
Internally rotated gait is not fully understood. In internally rotating moments, or compensatory internal
hemiplegic and diplegic cerebral palsy (CP) gait is often rotation for weak hip abductors [9,10].
characterised by ankle equinus, hip internal rotation and pelvic Characteristically in equinus gait, the triceps surae
retraction (external rotation) [1,2]. Pelvic retraction is muscle shows an onset of activation in late swing and a
commonly seen as a compensation for the increased internal prolonged, enhanced activity during stance [11,12]. The
hip rotation [3]. These proximal deviations, however, may effect of such overactivity on hip and pelvic position was
occur even when there is only calf muscle involvement. modelled for various positions of the leg in space using a
Interestingly, plantarflexion together with hip internal rotation forward dynamics simulation. It was hypothesised that
and pelvic retraction is also seen in patients with non-neurolo- overactive plantarflexors would result in hip flexion/internal
gical conditions, such as congenital absence of the anterior rotation and pelvic retraction. The clinical relevance of the
cruciate ligament or habitual toe walking. This suggests that results from this theoretical approach was then tested in
the underlying mechanism is not necessarily neurological. patients with hemiplegic and diplegic CP.
Results after surgical correction of femoral torsion for
internally rotated gait are sometimes disappointing [4–7] 2. Methods
which suggest a multifactorial origin of this problem. The
gait pattern itself has been accused but the study results 2.1. Modelling

2.1.1. General structure of the model


* Corresponding author. Tel.: +41 61 685 55 24; fax: +41 61 685 50 12. The model was composed of 13 geometrical solids representing
E-mail address: reinaldbrunner@dplanet.ch (R. Brunner). the main anatomical segments of the human body (Table 1). A

0966-6362/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2007.11.013
R. Brunner et al. / Gait & Posture 28 (2008) 150–156 151

Table 1 model because of their dynamic coupling. The displacement of the


Antropometric parameters of the human body model segments was computed by double integration (Kutta–Merson
Mass Mass Size numerical method) starting from the initial kinematic condition
ratio (%) (Kg) (m) and taking into account the ground reaction forces as an external
Whole body 100 45 h = 1.60 constraint. The ground reaction forces resulted from a ‘non-COM
Head 7.3 3.28 r = 0.10 penetration’ constraint between foot and ground. As a consequence
of the movement the spring representing the activated muscle
Trunk and pelvis 50.7 22.81
shortened and the force vanished to zero. The viscous damping
Trunk 34.4 15.70 l = 0.18 w = 0.30 h = 0.30
Pelvis 15.8 7.11 l = 0.12 w = 0.24 h = 0.16 coefficient of all the spring/damper elements was set to 1 Ns/m to
smooth out the movement and to achieve a new steady state without
Upper limb 4.9 2.20 oscillations.
Upper arm 2.6 1.17 r = 0.04 l = 0.28
Forearm and hand 2.3 1.03 r = 0.035 l = 0.30
Lower limb 16.1 7.24 2.1.3. Simulation conditions
Thigh 10.3 4.63 r = 0.06 l = 0.35 As a first condition gravity was excluded from our computation,
Shank 4.4 1.98 r = 0.045 l = 0.36 so that internal muscle forces were not required to keep the system
Foot 1.5 0.67 l = 0.24 w = 0.08 h = 0.06
in its static equilibrium. This assumption was justified by two
Mass ratio: percentage of segment mass in relation to body mass; h, height; reasons: (1) the induced acceleration depends on the force pertur-
r, radius; l, length; w, width. bation only, and so it is the same either if the system was in
equilibrium under gravity (which requires internal forces) or if it
was completely unloaded, (2) to compute the muscle forces in the
hypothetical subject, 160 cm tall, 45 kg of body mass, was con- presence of gravity (or any other loading condition) would require
sidered, and size and mass of anatomical segments were defined to assume a criterion of sharing the internal forces among the
according to Clauser et al. [13]. The mass density was uniform, so various muscles, because the system was mathematically undeter-
that centre of mass and central moments of inertia could be defined mined.
by simple geometrical calculations. A second condition was that all initial velocities and accelera-
A simulation software was used to implement the model and tions were set to zero so that the effect of the force perturbation was
to calculate the forward dynamics (Working Model 3D, MSC- interpreted as a deviation with respect to the previous, unperturbed
Software). The solid segments were connected by means of trajectory.
rotational constraints: spherical hinges at the shoulders and at The initial configuration of the model was defined to corre-
the hips (3 degrees of freedom), and cylindrical hinges at the spond with standing up-right posture, and to the conventional
elbows, knees and ankles (revolute joints, 1 degree of freedom). descriptors of stance phase [14]. The corresponding joint angles
Between the head and trunk and between the trunk and pelvis the were set to normal values for the sub-phases of stance phase and
upper segment was constrained to slide along an axis that was initial swing [14]. An exaggerated plantarflexion was simulated
hinged to the lower segment by a spherical joint. The relative producing forefoot ground contact to evaluate the effect of an
position of the upper and lower segments was controlled by four equinus ankle.
spring/damper elements. At time T = 0 the natural length of the spring representing the
The knee joint axes were oriented horizontally and parallel to soleus or the gastrocnemius was changed (reduced) by 50 mm. The
the coronal plane with a valgus of 58. The shank longitudinal axis stiffness of the spring was 200 N/m, and the resulting initial force
was vertical in standing position. The ankle axis was horizontal and 10 N. When the two muscles were activated simultaneously, the
perpendicular to the longitudinal foot axis which was externally stiffness of each one was reduced to 100 N/m to make the effect
rotated by 158. comparable to the single muscle contraction. The mechanical work,
DL = 1/2KDL2 corresponded to 0.25 J both in single and in simul-
2.1.2. Muscle actuators taneous muscle contraction.
The muscles were represented by mechanical spring/damper Similarly the effect of soleus and gastrocnemius was tested for a
elements. The two components of gastrocnemius were represented hypothetical configuration reproducing a typical crouch gait pos-
by just one of these elements, running from the thigh above the knee ture.
to the rear foot. The soleus was represented by another spring/ To assess the effects of the different muscles’ contractions,
damper element running from the shank to the same attachment pelvis and thigh orientation, knee and ankle joint angles, and foot
point of gastrocnemius on the rear foot. The origin and insertion of inclination in relation to the ground plane were analysed after
both gastrocnemius and soleus lay in the sagittal plane (soleus complete recoil of the spring (end of muscle contraction).
origin 0.02 m posterior to the longitudinal shank axis, 0.14 m distal
to the knee joint centre, gastrocnemius origin 0.06 m posterior to 2.2. Clinical study
the longitudinal thigh axis, 0.023 m proximal to the knee joint
centre; insertion of Achilles tendon 0.08 m posterior to, and, 0.06 m The hypothesis of a functionally short triceps resulting in hip
distal from the ankle joint centre). flexion/internal rotation and pelvic retraction was tested retrospec-
The activation of the muscles was simulated by shortening the tively in patients with hemiplegic or diplegic CP. Inclusion criteria
natural length of the spring. In this way the initial force abruptly to consider the affected leg were
rose to F = KDL (where K was the elastic constant and DL was the
change between the actual spring length and the new length). This  hemiplegic or diplegic CP,
force perturbation induced accelerations in all segments of the  a full instrumented standardised gait analysis,
152 R. Brunner et al. / Gait & Posture 28 (2008) 150–156

 equinus deformity (at least 58 of plantar flexion at initial contact Exclusion criteria were
as seen in 3 days gait analysis), and
 abnormal medial gastrocnemius activity in terminal swing from  previous Botulinum-toxin A injections within 6 months,
dynamic EMG raw data (the medial gastrocnemius was assumed  previous casting of the lower limbs within 12 months and
to be representative of triceps surae).  any previous surgical procedures.

All children were independent walkers. Forty-seven children had


spastic diplegia (80 involved legs, age 11.4  3.8 years, body mass
37.2  13.9 kg), 49 hemiplegia (49 involved legs, age 12.8  5.6
years, body mass 43.7  17.4 kg). All patients/parents gave written
consent for research purposes in accordance with local ethical
committee requirements.

2.2.1. Gait analysis


All patients underwent a full instrumented gait analysis between
the years 2000 and 2005, using a motion capture system (six camera
VICON 460 system, Oxford Metrics Ltd., UK), two force plates
(Kistler Instrumente AG, Winterthur, Switzerland) and an eight
channel surface EMG system (Zebris, Tübingen, Germany). The
patients walked at their self-selected speed. The Helen Hayes
Marker set [15] was used and at least six trials were recorded.
Anthropometric data were recorded for appropriate scaling. Sur-
face EMG was recorded simultaneously. Bipolar Ag/AgCl surface
electrode pairs (electrode diameter 10 mm and an inter-electrode
spacing of 22 mm) were placed bilaterally over the medial gastro-
cnemius, tibialis anterior, rectus femoris, and semitendinosus
muscles. For electrode placement, the SENIAM [16] recommenda-
tions for surface EMG were followed. The ground electrode was
placed over the tibial tuberosity. The EMG signals were band-pass
filtered (10–700 Hz) and collected at a sampling rate of 2500 Hz.
All data were expressed in percentage of gait cycle using the
Polygon software (Oxford Metrics Ltd., UK).

2.2.2. Data evaluation


Hip rotation, pelvic rotation and plantarflexion (mean values
over the whole stance phase and during mid-stance) were evaluated.
Mid-stance was studied because an increase of the plantar flexor
moment compared to normals is typically located during this phase.
Mean and standard error of the mean (S.E.M.) were calculated for
each parameter and each patient group (hemiplegics and diplegics)
and compared.

2.2.3. Statistical analysis


Spearman Rank Order Correlation coefficients were calculated
between the mean ankle plantarflexion and the pelvic rotation as
well as the mean hip rotation in stance and mid-stance, respectively,
for hemiplegics and for diplegics. Differences between the two
groups that could also influence the correlation between the equinus
deformity and the internal rotation gait pattern were identified by
multiple unpaired t-tests. The level of significance was set at
p = 0.05 for all statistical tests.

Fig. 1. Effect of single and simultaneous contraction of soleus and gastro- 3. Results
cnemius when the starting position is the one depicted in the first column
(gait phases: IC = initial contact, LR = loading response, MS = mid-stance, 3.1. Modelling
LS = late stance, PS = Preswing, TO = toe off). The first column of pictures
shows the position before muscle contraction according to the position of
segments in the gait phases, the following columns the resulting position of When the soleus contracted alone unilaterally, strong
the body segments after contraction of the muscle mentioned in the heading. plantarflexion and knee extension occurred (Fig. 1, Table 2).
Only the lateral view is shown. The hip was continuously adducted (maximum at late
R. Brunner et al. / Gait & Posture 28 (2008) 150–156 153

Table 2
Results from modelling
Leg position
After contraction Standing Initial contact Loading response Mid-stance Late stance Preswing Toe off
Soleus
Pelvic obliquity: up (up +) 5.91 2.3 3.71 5.73 9.7 7.24 4.48
Pelvic anterior tilt (ant. +) 3.57 3.5 4.03 2.23 0.842 5.06 3.92
Pelvic retraction (ext. rot. +) 15.2 12.9 14.5 19.4 11.2 6.76 10.4
Hip adduction (add. +) 6.75 1.91 3.83 6.93 11.8 8.04 5.58
Hip extension (ext. +) 12.73 8.7 10.13 11.33 7.092 9.26 13.92
Hip internal rotation (int. +) 8.04 9.23 20.22 15.7 3.97 5.37 13.89
Knee extension (ext. +) 0 4.94 4.96 0 2.02 10 17.87
Ankle plantarflexion (plantar +) 35.7 30.9 33.79 37.8 39.46 40.2 36.8
Gastrocnemius
Pelvic obliquity: up (up +) 1.36 0.249 0.398 1.01 1.54 0.78 0.969
Pelvic anterior tilt (ant. +) 3.68 3.24 3.32 3.3 3.07 2.57 1.82
Pelvic retraction (ext. rot. +) 14 11.8 11.9 13.1 10.7 10.9 8.04
Hip adduction (add. +) 2.86 3.119 3.438 5.51 5.54 3.08 3.069
Hip extension (ext. +) 26.18 19.24 21.62 24.1 23.97 25.07 19.4
Hip internal rotation (int. +) 18.41 29.7 27.7 33.5 28.4 18.66 14.35
Knee extension (ext. +) 32.3 21.66 26.54 35.8 37.18 36 27
Ankle plantarflexion (plantar +) 9.46 16.1 11.79 8.45 7.53 9.95 13.84
Soleus and gastroc.
Pelvic obliquity: up (up +) 6 2.03 3.05 6.94 9.4 5.96 4.17
Pelvic anterior tilt (ant. +) 3.6 3.93 4.43 2.57 1.89 1.38 0.515
Pelvic retraction (ext. rot. +) 15.7 15.5 17.2 18 15.7 11.9 5.58
Hip adduction (add. +) 6.88 1.63 3.98 8.04 11.7 9.66 7.57
Hip extension (ext. +) 13.17 14.23 19.93 11.36 18.89 29.28 20.875
Hip internal rotation (int. +) 7.34 20.33 27.3 14.49 22.33 18.83 13.21
Knee extension (ext. +) 0.127 3.6 13.04 0 17.58 37.2 26.6
Ankle plantarflexion (plantar +) 36.6 33.6 33.19 36.4 38.76 39.7 36.8

stance) and internally rotated (maximum at loading


response) and flexed (maximum at loading response), but
externally rotated and extended at Preswing and toe off. At
the pelvis it produced an elevation in all phases of gait. For
initial contact, loading response, mid-stance and late stance
there was pelvic retraction and anterior tilt while the
opposite was found at Preswing and toe off.
Gastrocnemius contraction resulted only in plantarflexion
(less than with soleus), knee and hip flexion, internal rotation
and adduction with a maximum for flexion and rotation
slightly later than for soleus (Fig. 1, Table 2). The pelvis was
anteriorly tilted and elevated. The same was true for
combined contraction of soleus and gastrocnemius (Fig. 1,
Table 2).
Knee flexion before simulated contraction partly
removed the proximal effects of the soleus and gastro-
cnemius contraction (Fig. 2).

3.2. Clinical study

Increased ankle plantarflexion over the whole stance


phase and during mid-stance correlated with increased
pelvic retraction in hemiplegics (r = 0.45, p = 0.001). The
Fig. 2. Model in crouch position. First column: initial condition; other
correlation between the mean ankle plantarflexion and columns: configurations attained at the end of activation of soleus, gastro-
internal hip rotation during stance (and mid-stance) was cnemius, and both muscles simultaneously. The same position is shown in
significant (r = 0.35, p = 0.009) for hemiplegics. In three different views for three-dimensional presentation.
154 R. Brunner et al. / Gait & Posture 28 (2008) 150–156

Fig. 3. Sagittal and transverse kinematics comparing both groups; mean values of all involved legs of the hemiplegic (solid black line), the diplegic patients
(dashed black line) as well as the age matched-norm children (solid grey line) in respect to the gait cycle (x-axis) are displayed. Significant deviations ( p < 0.05)
between the hemiplegic and diplegic children are shown by the hatched bar below the curves. Positive values on the y-axis represent hip flexion (a), knee flexion
(b), dorsiflexion (c) and internal rotation (d + e). The vertical lines represent the transition from stance to swing phase.

contrast, mean plantarflexion in stance showed neither influences on the pelvic and hip rotation effect are not to be
significant correlation with internal hip rotation nor with expected. Differences in kinematics between the two groups
pelvic retraction in diplegics, as well as for the evaluation are displayed in Fig. 3. Whereas no significant differences
during mid-stance. could be found for hip rotation ( p = 0.843), the hemiplegic
Hemiplegics showed significantly less anterior pelvic tilt group showed significantly more pelvic retraction
compared to diplegics during the first 25% of the gait cycle ( p = 0.002). An increased internal foot progression angle
( p < 0.050). Increased hip flexion during stance was only was found in diplegics ( p = 0.001), whereas hemiplegics
found in diplegics. Knee flexion at initial contact showed an almost normal foot progression angle. The ankle
( p < 0.001) and during loading response ( p = 0.013) was plantar flexor moment and power absorption ( p = 0.040)/
significantly higher in diplegics. In comparison to hemi- generation ( p < 0.001) was significantly greater in hemi-
plegics, who reached normal knee extension during mid- plegics.
stance and terminal stance, there was insufficient knee
extension in diplegics. There were no significant differences
in plantar flexion during the whole stance phase ( p = 0.443) 4. Discussion
between the two groups. The mean plantar flexion at initial
contact in hemiplegics was 48 higher than in diplegics, but In CP hip internal rotation is often combined with pelvic
this difference was not significant ( p = 0.186). Hence, retraction, and hip and pelvic motions are interpreted as
R. Brunner et al. / Gait & Posture 28 (2008) 150–156 155

compensating for each other. Excessive plantarflexion is a that in hemiplegics. There may be several reasons for this.
frequent concomitant deviation. These deviations at hip and First, there may be other factors still unknown that cause hip
pelvis are seen, as expected, in Type 4 hemiplegic patients internal rotation, adduction and abnormal pelvic motion in
but also in Type 2 ones with no neurological involvement at diplegics. Secondly, there may be other biomechanical
hip level [17]. The combination of plantarflexion, hip factors that partially or completely prevent the effect of the
internal rotation and pelvic retraction can also be found in triceps surae on the hip and pelvis. In this study, one possible
other, non-neurological conditions. Correcting the increased explanation is the increased flexion of knee and hip in the
femoral anteversion, adductor and tensor fasciae lata diplegics, compared to the hemiplegics. This hypothesis is
spasticity in CP surgically is not always effective in supported by the results of the model, where flexion erased
controlling hip internal rotation during gait. Discrepancies the effect of triceps surae overactivity. Thirdly, bilateral
between the intraoperative amount of femoral derotation and involvement may remove part of these effects as the opposite
the functional outcome have been reported [3,6]. Hence effect occurs on the contralateral side. Fourthly, diplegics
additional causes for hip internal rotation during gait need to showed significant foot malalignment with reduced moment
be considered. and power production/absorption at the ankle. This may be
The causes of functional hip internal rotation in CP may due to the triceps acting out of plane.
be difficult to determine as gait patterns are subject to In conclusion, our model showed that excessive ankle
compensations and secondary effects. A biomechanical plantarflexion was responsible for flexion, internal rotation
model may help: in the present study the model simulated and adduction at the hip, as well as pelvic retraction and
soleus and gastrocnemius function and included floor upward motion of the pelvis. The model suggests that these
resistance and dynamic coupling between anatomical effects were not compensatory movements. These effects
segments. contributed to the hip and pelvic deviations in the
Our model allowed testing the effect of the triceps surae hemiplegic patients, whereas other factors, such as knee
components under various conditions of load and positions and hip flexion and foot malalignment may have prevented
of flexion at the ankle, knee, hip and spine. In our simulation this effect in diplegics. The model also showed that soleus
results, each component of the triceps surae muscle flexed, contraction produced knee extension whereas gastrocne-
internally rotated and adducted the hip and displaced the mius contraction resulted in knee flexion. This may be of
pelvis backwards and upwards. This was particularly relevance clinically. Correction of triceps surae function
noticeable in early stance when triceps surae overactivity requires careful consideration when internally rotated gait is
is typical in CP [2,11,18]. In contrast, a contraction of soleus corrected in hemiplegia.
alone in late stance had the opposite effect on the body
segments. Hence hip and pelvic motions, especially the
rotational component, were a result of triceps surae Acknowledgements
contraction under load. This model suggests that the pattern
of internal hip rotation and pelvic retraction does not The authors like to acknowledge the Foundation for
necessarily occur as a compensation, which has been often Movement Disorders (Stiftung fuer Bewegungsstoerungen)
assumed in CP. However, at knee level, the soleus extended and the research project HINT@Lecco for their financial
the joint whilst gastrocnemius flexed it. This is in keeping support of this study.
with the concept of soleus controlling stance stability. This Conflict of interest: None.
model suggests that effects at the hip and knee are related to
the function of the triceps surae and are not directly
dependent on neuromuscular control. References
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