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Article history: Hip rotation from gait analysis informs clinical decisions regarding correction of femoral torsional
Received 25 September 2015 deformities. However, it is among the least repeatable due to discrepancies in determining the medial-
Received in revised form 4 February 2016 lateral axis of the femur. Conventional or functional calibration methods may be used to define the axis
Accepted 5 February 2016
but there is no benchmark to evaluate these methods. Freehand 3D ultrasound, the coupling of
ultrasound with 3D motion capture, may provide such a benchmark.
Keywords: We measured the accuracy in vitro and repeatability in vivo of determining the femur condylar axis
Freehand 3D ultrasound
from freehand 3D ultrasound. The condylar axis provided the reference medial-lateral axis of the femur
Anatomical femur coordinate system
and was used to evaluate one conventional method and three functional calibration methods, applied to
Condylar axis
Gait analysis three calibration movements. Ten healthy subjects (20 limbs) underwent 3D gait analysis and freehand
Functional calibration 3D ultrasound. The functional calibration methods were a transformation technique, a geometrical
method and a method that minimises variance of knee varus-valgus kinematics (DynaKAD). The
conventional method used markers over the femoral epicondyles.
The condylar axis determined by 3D ultrasound showed good accuracy in vitro, 1.68 (SD: 0.38) and
good repeatability in vivo, 0.28 (RSMD: 2.38). The DynaKAD method applied to the walking calibration
movement determined the medial-lateral axis closest to the ultrasound reference. The average angular
difference in the transverse plane was 3.18 (SD: 6.18).
Freehand 3D ultrasound offers an accurate, non-invasive and relatively fast method to locate the
medial-lateral axis of the femur for gait analysis.
ß 2016 Elsevier B.V. All rights reserved.
1. Introduction plane of the femur anatomical coordinate system. The frontal plane
of the femur is defined by the cross-product of its longitudinal axis
Gait analysis provides quantitative information of a subjects (hip joint centre to knee joint centre) and its medial-lateral axis. It
gait pattern in the form of joint angles, moments and powers. In the is the difficulty in determining the medial-lateral axis of the femur
clinical setting, it informs decision making regarding surgical that affects hip rotation kinematics [4]. Conventional gait models,
correction of gait deformities. For example, the hip rotation profile widely implemented in commercial software packages (e.g. Plug in
during gait is a major determinant in recommending femoral Gait, Vicon motion systems, Oxford UK), define the medial-lateral
derotation osteotomy and in predicting functional outcomes axis of the femur by the transepicondylar axis. This axis is
[1]. However, hip rotation kinematics has been found to be among identified by placement of markers over the medial and lateral
the least repeatable data from gait analysis [2–4]. epicondyles of the femur, or the positioning of a Knee Alignment
The lack of repeatability of the hip rotation profile can primarily Device (KAD) which clamps on the medial and lateral epicondyles
be attributed to a lack of repeatability in determining the frontal [5].
Alternatively, several functional calibration methods have been
proposed. These use the motion of the femur and the tibia during a
* Corresponding author at: The Royal Children’s Hospital Melbourne 50 Fle-
calibration movement to determine the axis that best describes the
mington Road Parkville Victoria 3052 Australia. Tel.: +61 3 9345 5354.
E-mail addresses: elyse.passmore@gmail.com, elyse.passmore@rch.org.au flexion–extension movement of the knee joint. The knee axis is
(E. Passmore). then used, explicitly [4,6] or implicitly [7], as a proxy to define the
http://dx.doi.org/10.1016/j.gaitpost.2016.02.006
0966-6362/ß 2016 Elsevier B.V. All rights reserved.
212 E. Passmore, M. Sangeux / Gait & Posture 45 (2016) 211–216
medial-lateral axis of the femur. These methods have the Each subject underwent 3D gait analysis and freehand 3D
advantage of removing the need for precise marker placement ultrasound imaging of the posterior aspect of the femoral condyles.
over anatomic landmarks but may be sensitive to the type of The gait analysis protocol consisted of a static standing calibration,
calibration movement and soft tissue artefact between the skin- functional calibration movements, and walking at self-selected
mounted markers and the underlying bones. The majority of speed. Passive reflective markers were attached to the subject
functional calibration methods model the movement of the knee according to the Plug-in-Gait marker set [22] (Vicon Motion
by a fixed single axis of rotation. This is seen in axis transformation Systems) with additional markers on the thigh and shank, Fig. 2(a).
techniques (ATT or SARA) [8] as well as in geometrical methods An experienced tester (EP) performed marker placement for each
[6,8–10]. An alternative to the single axis of rotation approach are subject.
those methods which determine an axis which minimises the We defined the medial-lateral axis of the femur as the condylar
variance of the frontal plane (varus\valgus) knee kinematics [4,11– axis [23,24]. The condylar axis models the posterior aspect of the
13]. These methods assume the variance is a result of cross-talk medial and lateral condyles as spherical or cylindrical. The medial-
from the sagittal plane movement. lateral axis of the femur is defined by the line connecting the
Validation of the methods to define the medial-lateral axis of centres of the medial and lateral spheres/cylinders that best fit the
the femur are limited due to the absence of a benchmark able to posterior aspects of the condyles [25,26]. In our freehand 3D
provide the respective position of the femur anatomical coordinate protocol, we used the most posterior aspect of the condyles which
system to the skin-mounted markers. Currently, validation has were identified with the subject standing, Fig. 2(b). The probe was
been limited to in silico data [8,10], mechanical or surrogate models positioned over the knee popliteal fossa in a medial-lateral
[14], or in vivo data with indirect outcome measures such as inter-/ orientation, the image depth was set at 60 mm with focus between
intra-assessor repeatability of the hip and knee kinematics or the 20 and 30 mm. The probe was moved up and down to identify the
absence of cross-talk [4,6,7]. most posterior aspect of each condyle. The freehand 3D ultrasound
Coordinate systems that are anatomically sound (coordinate images were loaded into the software Stradwin [15] and two
systems that match the bone/segment planes) and repeatable are landmarks were positioned manually to locate the most posterior
required to ensure accurate gait analysis results. We hypothe- aspect of the condyles, Fig. 2(c). For some subjects it was
sized that a freehand 3D ultrasound method may be used to impossible to view both condyles simultaneously and separate
define an anatomical coordinate system of the femur that is more images and landmarks were obtained for the medial and lateral
accurate and repeatable than conventional and functional condyles.
calibration methods. Freehand 3D ultrasound combines ultra- The conventional method utilised markers over the medial and
sound imaging with 3D motion capture [15] and has been lateral epicondyles to define the medial-lateral axis of the femur,
utilised in gait analysis to determine the location of the hip joint Fig. 2(a). Three functional calibration methods were tested, each
centres [16–18]. Freehand 3D ultrasound allows for the position applied to three different calibration movements. The calibration
of the bones to be determined in relation to the skin-mounted methods were: the ATT [8], which determines the knee axis that
markers. We propose to use the most posterior aspects of the moves the least during the calibration movement, the geometric
medial and lateral condyles to define the medial-lateral axis of method of Chang and Pollard [10], which assumes marker
the femur. This corresponds to the table top axis described by trajectories form concentric circles around the knee flexion axis
Murphy and Simon [19] for measuring femoral torsion, also and the DynaKAD method [4,11], which minimises variance in the
called femoral anteversion, and to the condylar axis presented by frontal plane (varus\valgus) knee kinematics. The calibration
Eckhoff et al. [20]. movements were three repetitions of active knee flexion–
The objectives of this study were (1) to determine in vitro extension (open kinematic chain), bilateral squats (closed kine-
the accuracy of the freehand 3D ultrasound system to locate matic chain) and walking strides at a self-selected speed. Markers
the medial and lateral condyles, (2) to determine in vivo the on the thigh and the shank (Fig. 2(a)) were tracked using least
repeatability of defining an anatomical coordinate system of the squares fitting [27] for the functional calibration methods.
femur using freehand 3D ultrasound imaging and (3) to use The reference anatomical coordinate system of the femur was
the anatomical coordinate system of the femur from freehand 3D determined as follows. The primary axis was the longitudinal axis
ultrasound as a benchmark to evaluate conventional and of the femur (Z- axis) and defined by the vector from knee joint
functional methods commonly used in gait analysis. centre to hip joint centre. The positions of the hip and knee joint
centres were determined from the static calibration using Plug-in-
2. Methods Gait (Vicon motion systems). The anterior-posterior axis (X- axis,
perpendicular to the frontal plane of the femur) was determined by
Five reflective markers were rigidly attached to a 59 mm Echo the cross-product of the longitudinal axis and the medial-lateral
Blaster 128-1Z ultrasound probe (Telemed, Lithuania). The axis of the femur as identified by freehand 3D ultrasound imaging.
coordinate system of the probe was built from the marker The Y- axis of the femur was defined as the cross-product between
positions and the pose of the probe tracked using least squares the Z- and X- axes, which corresponds to the medial-lateral axis
fitting [21]. A calibration procedure using the Cambridge stylus projected onto the transverse plane of the femur.
method was performed to determine the position of the Similar coordinate systems of the femur were constructed for
ultrasound image in the coordinate system of the probe the conventional and functional methods. For all methods, the
[18]. A ten-camera video-motion-capture system (Vicon Motion longitudinal axis of the femur coordinate system was the same
Systems) recorded marker positions at 100 Hz and a radio because the locations of the hip and knee joint centres were held
frequency button triggered the motion-capture and ultrasound constant. However, each conventional or functional method led to
systems simultaneously. a different estimate of the medial-lateral axis of the femur and
Ten healthy adults (5 males, 5 females), mean age 29 9 years therefore led to a different frontal plane of the femur. The
and BMI of 24.4 3.1 kg/m2 with no history of gait pathology, joint conventional and functional calibration methods were compared
disease, injury or neurological problems were recruited to evaluate to the freehand 3D ultrasound method as the reference. The
the freehand 3D ultrasound protocol in vivo. The participants gave angular difference between the frontal planes of the femur was
written informed consent and ethics approval for the study was calculated for each method\calibration movement. This angular
granted from the local institutions ethics committee. difference reflects the offset in hip rotation that would be observed
E. Passmore, M. Sangeux / Gait & Posture 45 (2016) 211–216 213
between the methods. Results were calculated for both knees of ultrasound protocol was performed three times with the examiner
each subject (20 samples). The hip and knee joint kinematics for blinded to the location of the femur within the container, Fig. 1(b).
each subject during a representative gait cycle were calculated Two markers attached to the femur defined its shaft axis. The
using the femur coordinate system from each method/calibration angular difference between the condylar axes defined from the
movement combination. The pelvic and tibia coordinate system of Cambridge stylus and from freehand 3D ultrasound was calculated
each subject remained constant for all methods. in the plane perpendicular to the shaft axis of the femur.
The results were compared to the variability of the hip rotation All statistical analyses were performed in Minitab (Minitab Inc.,
kinematics from our subjects a posteriori. The standard deviation of State College, USA).
hip rotation kinematics was 7.78 in our dataset. We considered that
results farther than 15.48 (2 standard deviations) from the 3. Results
reference method may affect clinical decision making. We therefore
reported the proportion of the results within 15.48 of the reference The angular difference between the axes obtained in vitro from
method for each method/calibration movement combination. The the freehand 3D ultrasound protocol and the Cambridge stylus was
results were analysed through a general linear model ANOVA with the 1.68 (SD: 0.38). In vivo, the repeatability of the freehand 3D
following two fixed effects: calibration method (ATT, Geometric and ultrasound protocol was good with average difference between
DynaKAD) and calibration movement (flexion–extension, bilateral repeated measures of 0.28 (RMSD: 2.38). Results for all methods
squats and walking). Tukey’s simultaneous tests and grouping and calibration movements are presented in Fig. 3. The general
analysis was performed post hoc to determine the difference between linear model ANOVA results showed a significant effect (p = 0.037)
methods at a = 0.05. for interaction of the functional calibration method and calibration
The repeatability of the freehand 3D ultrasound method was movement. The DynaKAD method consistently produced the
estimated in vivo. Two separate acquisitions of ultrasound data and results closest to the ultrasound reference, walking calibration
identification of the posterior aspect of the condyles were movement average difference: 3.18 (SD: 6.18). All data using
performed for each knee and the angular difference in the DynaKAD with the walking calibration movement were within the
transverse plane between the two measurements calculated. range of hip rotation variability of our data set. The conventional,
We estimated the accuracy of the freehand 3D ultrasound ATT and geometric methods all resulted in axes that were
protocol in vitro. The femur was positioned on a level surface with predominantly external compared to the ultrasound reference.
the shaft of the femur horizontal to the surface and an inkpad Details of the range of motion achieved for each of the
under the condyles. As a result, the ink marked the most posterior functional calibration movements can be found in Table 1. Similar
aspects of the condyles corresponding to the anatomical axis (table amounts of knee varus and knee rotation were observed for all
top axis) described by Murphy and Simon [19], Fig. 1(a). The femur movements. The walking movement produced a reduced range of
was then firmly secured to a rigid container. Three markers, placed knee flexion 708 (SD: 48) compared to the flexion–extension 1088
on the outside, defined the container’s coordinate system. We (SD: 308) and bilateral squats 1068 (SD: 158) movement.
obtained the reference coordinates of the medial and lateral Kinematic curves for the knee (sagittal and frontal planes) and
condyles with respect to the container’s coordinate system by the hip (transverse plane) during a representative gait cycle for
pointing to the centre of the ink areas with the Cambridge stylus. each limb are shown in Fig. 4. The graphs show the group average
The container was then filled with water and the freehand 3D plus and minus one standard deviation. The ultrasound reference
method had on average, 5.78 (SD: 7.78) of internal hip rotation
throughout the gait cycle and minimal variance in knee varus/
valgus. The DynaKAD method consistently produced group
averages closest to the ultrasound reference method. The ATT
and geometric methods were consistently further away. In
particular, using the bilateral squats calibration movement, the
knee kinematics showed a marked valgus dip during knee flexion
consistent with cross-talk at the knee for both methods.
4. Discussion
Fig. 2. (a) Marker set definition; The four markers on the thigh and the three markers on the shank (blue) were used to track segments during functional calibration
movements; Medial and lateral epicondyle markers were used to define the transepicondylar axis of the conventional method (red). (b) Subject during 3D freehand
ultrasound imaging of the posterior aspect of the condyles. The femoral coordinate system was defined as follows. The primary axis (blue) was the longitudinal axis of the
femur (Z- axis) defined by the vector from knee joint centre to hip joint centre. The hip and knee joint centres are marked by &. The anterior–posterior axis (red) (X- axis,
perpendicular to the frontal plane of the femur) was determined by the cross-product of the longitudinal axis and the medial–lateral axis of the femur (dashed green) as
identified by freehand 3D ultrasound imaging. The Y- axis of the femur (green) was defined as the cross-product between the Z- and X- axes, which is the medial-lateral axis
projected onto the transverse plane of the femur. (c) Ultrasound image of the posterior aspect of the condyles, the crosses identify the landmarks placed to represent the most
posterior aspect of the condyles. The medial–lateral axis of the femur is represented by the dashed green line.
with average difference between repeated measures of 0.28 knee flexion–extension axis, and the condylar axis the authors
(RMSD: 2.38). found minimal angular difference between the condylar axis and
We used the most posterior aspects of the medial and lateral the knee flexion–extension axis, 18 (38 with the transepicondylar)
condyles to define the medial-lateral axis of the femur. This in the transverse plane. In addition, Johal et al. [30] found that tibial
corresponds to the table top axis described by Murphy and Simon rotation was facultative rather than obligatory over the 208–908 arc
[19] for measuring femoral torsion, and the condylar axis of knee flexion. This supports an overall understanding of the
presented by Eckhoff et al. [20]. There is a growing body of movement at the knee being decoupled in terms of sagittal plane
literature supporting the condylar axis as a bone-fixed surrogate knee flexion–extension and internal–external tibial rotation.
for the sagittal plane flexion–extension axis of the knee [25,28– The use of an anatomical definition of the femur coordinate
30]. For example, in Hancock et al. [24], the authors advocate the system is also essential to support clinical interpretation of hip
use of the condylar axis for the positioning of the knee prosthesis, rotation kinematics during gait and to inform clinical decision on
which has a single-fixed axis of rotation. Recently Yin et al. [31] femoral de-rotation osteotomy. We used the condylar axis
utilised a bi-plane X-ray system to compare the orientation of the determined from freehand 3D ultrasound as a reference for the
medial-lateral axis of the femur. We used this reference to evaluate
several conventional and functional methods commonly employed
in gait analysis. Results showed that the DynaKAD method was
consistently the closest to the ultrasound reference. Nearly all
results from the DynaKAD method were within the variability
(2SD) of hip rotation of our dataset for the flexion–extension (95%),
squats (100%) and walking (100%) calibration movements,
Fig. 3. Therefore, data for which only walking is available may be
calibrated using the DynaKAD functional axis. In populations with
walking disabilities the range of knee flexion during walking may be
reduced compared to the population we investigated in this study. For
these populations we anticipate the need for additional, and probably
assisted, knee flexion–extension movement.
The conventional method uses the transepicondylar axis and
was predominantly external compared to the freehand 3D
ultrasound condylar axis. Eighty percent of the results from the
Table 1
Range of movement for the knee joint during functional calibration movements.
Fig. 3. Boxplot of the angular difference from the 3D freehand ultrasound reference
for 20 limbs. Proportion of data in % within 15.48 (2 SD of the variability of hip Calibration movement Knee flexion (8) Knee varus (8) Knee rotation (8)
rotation in our subjects) of the ultrasound axis is displayed at the top of the graph.
Flexion–extension 108 30 11 5 18 9
Tukey’s grouping results (a = 0.05) are specified at the bottom of the graph, each letter
Bilateral squats 106 15 11 4 25 8
specifies a statistically separate group from (A) closest to the 3D freehand ultrasound
Walking 70 4 13 4 24 3
reference to (D) furthest. * represents outlying data points. Signifies the mean.
E. Passmore, M. Sangeux / Gait & Posture 45 (2016) 211–216 215
Fig. 4. Kinematic curves for knee flexion, knee varus and internal hip rotation during one gait cycle. Data presented as group average plus and minus one standard deviation for
each method. The values presented alongside the internal hip rotation graphs are the value of the group average at the last time point. By construction, the hip rotation offset
between the groups remains constant throughout the gait cycle.
conventional method were within the hip rotation variability from with 5 years’ experience but who rarely performs clinical marker
our data set. The transepicondylar and condylar axes may not be placement. We cannot exclude that improved results may have
parallel anatomically. Studies, using a range of medical imaging been obtained with an assessor who is more frequently involved in
techniques, found the two axes to have an angular difference clinical marker placement. However, even when performed by
between 28 to 78 [20,32]. It is therefore likely that the difference we experienced gait analysis personnel, the accuracy and repeatability
measured was due to inaccuracy in marker placement rather than of marker placement may still be an issue [2–4]. A limitation of our
genuine anatomical difference between the transepicondylar and study is the use of a small sample of 10 healthy adults (20 limbs) to
condylar axes. Marker placement was performed by a gait analyst calculate the standard deviation of the hip rotation kinematics.
216 E. Passmore, M. Sangeux / Gait & Posture 45 (2016) 211–216