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The Knee 21 (2014) 688–693

Contents lists available at ScienceDirect

The Knee

Effect of lower limb malalignment in the frontal plane on transverse


plane mechanics during gait in young individuals with varus
knee alignment
Felix Stief a,⁎, Harald Böhm b, Chakravarthy U. Dussa b, Christel Multerer b, Ansgar Schwirtz c,
Andreas B. Imhoff d, Leonhard Döderlein b
a
Orthopedic University Hospital Friedrichsheim gGmbH, Frankfurt/Main, Germany
b
Orthopedic Hospital for Children, Aschau i. Chiemgau, Germany
c
Department of Biomechanics in Sport, Technical University, Munich, Germany
d
Department of Orthopedic Sports Medicine, Technical University, Munich, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Background: Varus knee alignment has been identified as a risk factor for the progression of medial knee osteo-
Received 20 June 2013 arthritis (OA). This study tested the hypothesis that not only frontal plane kinematics and kinetics but also trans-
Received in revised form 4 March 2014 verse plane lower extremity mechanics during gait are affected by varus malalignment of the knee.
Accepted 11 March 2014 Methods: Eighteen, otherwise healthy children and adolescents with varus malalignment of the knee were stud-
ied to examine the association between static varus malalignment and functional gait parameters. Kinematic data
Keywords:
were collected using a Vicon motion capture system (Vicon Motion Systems, Oxford, UK). Two AMTI force plates
Gait analysis
Varus malalignment
(Advanced Mechanical Technology, Inc., Watertown, MA, USA) were used to collect kinetic data.
Knee osteoarthritis Results: The results indicated that changes in transverse plane mechanics occur concomitantly with changes in
Knee adduction moment knee malalignment in the frontal plane. A mechanical consequence of varus knee malalignment is obviously
Internal tibia rotation an increased endorotation of the foot (internal foot placement) and an increased internal knee rotation (tibia
rotation) during stance phase. The linear correlation between the maximum external knee adduction moment
in terminal stance and the internal knee rotation in terminal stance (r = 0.823, p b 0.001) shows that this trans-
verse plane gait mechanics is directly in conjunction with intrinsic compressive load on the medial compartment
during gait.
Conclusions: Understanding factors that influence dynamic knee joint loading in healthy, varus malaligned knees
may help us to identify risk factors that lead to OA. Thus, three-dimensional gait analysis could be used for clinical
prognoses regarding the onset or progression of medial knee OA.
© 2014 Elsevier B.V. All rights reserved.

1. Introduction adduction moment is used as the primary parameter for characterizing


intrinsic compressive load and articular cartilage degeneration in the
Mechanical factors, such as varus malalignment of the knee in the medial knee compartment during gait [4,5,9,10].
frontal plane, have been implicated in the progression of medial knee Previous studies have investigated biomechanical changes during
OA [1–6]. A recent study by Hayashi et al. [6] has shown that varus gait in the sagittal and frontal planes in patients with knee OA compared
knee alignment is associated with increased risk of incidence and to healthy controls [5,11,12]. For example, patients with medial knee OA
enlarging bone marrow lesions. Quantitative gait analysis as an adjunct make initial contact with the ground with the knee in a more extended
to static radiographic measures of alignment provides an estimate of position and have a smaller range of knee flexion during the stance
tibiofemoral load through an inverse dynamic analysis and can be phase of walking [11]. However, these studies on patients with
used to gain a better understanding of the biomechanical factors that established knee OA have made it difficult to determine if biomechani-
contribute to the pathogenesis of knee OA [7,8]. The external knee cal changes are involved in the development of disease, are in response
to degenerative changes in the joint, or are compensatory mechanisms
in response to these degenerative changes or to joint pain.
⁎ Corresponding author at: Orthopedic University Hospital Friedrichsheim gGmbH,
In children and adolescents with varus malalignment of the knee
Marienburgstraße 2, 60528 Frankfurt/Main, Germany. Tel.: +49 69 6705 862. without signs of knee OA abnormally increased knee internal rotation
E-mail addresses: felix.stief@gmx.de, f.stief@friedrichsheim.de (F. Stief). and hip external rotation moments were detected [13]. While transverse

http://dx.doi.org/10.1016/j.knee.2014.03.004
0968-0160/© 2014 Elsevier B.V. All rights reserved.
F. Stief et al. / The Knee 21 (2014) 688–693 689

plane mechanics can initiate degenerative changes to the articular carti- gave verbal assent to study participation, and their parents provided
lage and have been implicated in the progression of knee OA [10], there is written informed consent to participate in this study, as approved by
a lack of research on the relationship between static varus malalignment the local ethics committee and in accordance with the Helsinki
of the knee and transverse plane lower extremity mechanics during gait. Declaration.
In particular, it is still not known which role the rotational gait profile
plays in the progression of knee OA. The purpose of the present study 2.2. Gait analysis methods
was therefore to investigate the effect of pathological varus alignment
of the knee on transverse plane gait parameters of the lower extremity Three-dimensional gait analysis was carried out using a Vicon mo-
in young individuals without signs of knee OA. The following question tion capture system (Vicon Motion Systems, Oxford, UK) operating
should be answered and may have important implications for the pro- at a sampling rate of 200 Hz (Fig. 1). The level walkway was 15 m
gression of knee OA: Does a relationship exist between static lower ex- long and viewed by eight infrared cameras. Two AMTI force plates
tremity malalignment in the frontal plane and transverse plane lower (Advanced Mechanical Technology, Inc., Watertown, MA, USA) were
extremity mechanics during gait? We hypothesized that (1) the static situated at the mid-point of the walkway to collect kinetic data at
varus alignment of the knee correlates with internal knee rotation (tibial 1000 Hz.
rotation) and endorotation of the foot (internal foot placement) during To improve the reliability and accuracy when analyzing frontal and
the stance phase of gait, and (2) the rotational gait profile has an influ- transverse plane gait data, a custom made lower body protocol
ence on the external knee adduction moment and thus also leads to de- described in a previous investigation [16] was used. In addition to the
generative changes in the knee joint in young patients with varus standardized Helen Hayes marker set [17], reflective markers on the
malalignment of the knee. medial malleolus, medial femoral condyle and major trochanter were
applied to determine positions of joint centers of rotation for the hip,
2. Methods knee and ankle. In contrast to the Helen Hayes marker set [17], the cen-
ters of rotation for the knee and ankle joints were defined statically as
2.1. Subjects the midpoint between the medial and lateral femoral condyle and
malleolus markers. This eliminates the reliance on the subjective palpa-
Eighteen, otherwise healthy children and adolescents with varus tion of the thigh and tibia wand markers, which is difficult to handle and
malalignment of the knee 12–19 years of age were consecutively select- less reliable within or between therapists than manual palpation [18].
ed during clinical visits between January 2008 and October 2012 The center of the hip joint was calculated using a geometrical prediction
(Table 1). Solely patients were included with a clinical indication for a method [17]. The major trochanter marker was used to improve the
full-length standing anteroposterior radiograph and a pathological prediction of the hip joint center by immediately calculating the dis-
varus alignment of at least one knee according to the mechanical axis tance between the anterior superior iliac spine and the major trochanter
angle (MAA) of the lower limb [14]. Alignment was defined as patholog- by anatomical landmarks [16]. Varus/valgus alignment of all knee joints
ical varus when the angle was more than 1.3° [14]. Patients were was determined by rotating the local shank coordinate system about the
excluded if they had signs of OA or rheumatoid arthritis, anterior cruci- y-axis of the thigh (vector from the lateral knee to the medial knee)
ate ligament (ACL) deficiency, neuromuscular dysfunction, achondro- until the x-axis of the shank (vector from the knee center to the ankle
plasia, sagittal or transverse plane deformities of the leg, flexion center) fell in line with the x-axis of the thigh (vector from the knee cen-
contractures in the knee or hip joint, leg length discrepancy of more ter to the hip center). According to Hunt et al. [7] using the same marker
than 1 cm, avascular necrosis, history of major trauma or a sports injury set for a similar purpose, this varus angulation provided an accurate,
of the lower extremity, knee surgery within the last 12 months, chronic marker-based measure of lower limb alignment in the frontal plane. It
joint infection, intraarticular corticosteroid injection, or morbid obesity has been shown that adding these few extra markers to the standard
according to the body mass index [15]. Helen Hayes marker set increases the repeatability in three-
Fifteen healthy subjects were recruited as control group (Table 1). dimensional gait analysis, reduces the measurement errors when ana-
All subjects had undergone a clinical examination, including passive lyzing frontal and transverse plane gait data, and improves the accuracy
hip, knee and ankle range of motion (Table 1). The patients and the of the knee joint axis by reducing the knee axis cross-talk phenomenon
healthy subjects had normal strength and full range of motion in the [16,19,20]. Furthermore, our lower body protocol enables the detection
lower extremities. of significant effects in the tibiofemoral angles and moments in the fron-
All subjects, and their parents in the case of subjects under age 18, tal and transverse plane between three different patterns of movement
were thoroughly familiarized with the gait analysis protocol. Subjects [21]. Further processing incorporating force plate data allowed external
18 and over gave written informed consent. Subjects younger than 18 moments (normalized to body weight) about the mathematically
derived joint centers to be calculated.
Discrete variables of interest (Table 2) were calculated for five bare-
Table 1
foot trials at a self-selected speed and then averaged for further analysis
Study population characteristics (mean with standard deviation in parenthesis) and p-values.
on the basis of complete marker trajectories and a clear foot-forceplate-
Variable Patients Controls p -value contact. In the case of bilateral involvement, measurements were per-
n 18 15 formed only on the limb with greater malalignment. This ensures that
Sex, no. female/no. male 11/7 9/6 the statistical calculations were independent from each other. No signif-
Age, years 15.2 (1.8) 15.1 (4.3) 0.941 icant differences were found in the discrete variables of interest
Height, m 1.64 (0.18) 1.64 (0.15) 0.973
Body mass, kg 55.7 (11.2) 52.8 (12.8) 0.502
comparing the left and right sides in the control group. Therefore, only
Body mass index, kg/m2 20.6 (3.0) 19.2 (2.2) 0.144 one side – the left side was chosen here – was used for further analysis
Max. passive internal hip rotation 44.3 (13.7) 45.8 (3.6) 0.690 of the controls.
(prone, hip neutral, knee flexed 90°), ° After each acquisition session, missing frames were handled with
Max. passive external hip rotation 37.0 (14.6) 41.3 (3.1) 0.290
a fill-gap procedure using the Vicon-Nexus software version 1.7.1
(prone, hip neutral, knee flexed 90°), °
Max. passive tibial torsion −12.0 (10.5) −12.9 (4.5) 0.763 (Vicon Motion Systems, Oxford, UK). The data were smoothed with a
(prone, hip neutral, knee flexed 90°), ° Woltring filter and using a smoothing spline [22]. The external knee
Self-selected walking speed, m/s 1.25 (0.10) 1.28 (0.11) 0.431 adduction moment as well as the transverse plane gait parameters dur-
Mechanical axis angle, ° 10.3 (7.0) ing stance phase were automatically determined by a custom made
External foot rotation (tibial torsion) is negative. algorithm in Matlab 7.12.0 (The MathWorks, Inc., Natick, MA).
690 F. Stief et al. / The Knee 21 (2014) 688–693

a b c
Fig. 1. Gait analysis methods: reflective markers (a), infrared camera (b), computerized body model (c).

According to Perry [23], loading response was defined as a subphase of frontal plane. This enables comparison between these two measure-
the gait cycle, i.e. 2–12% of the gait cycle. This phase follows the initial ments and can be used as quality assurance of the marker-based
contact of the foot with the floor and continues until the contralateral lower body protocol.
limb is lifted for swing. Mid stance (12–31% of the gait cycle) begins
as the contralateral foot is lifted and continues until body weight is 2.4. Statistical analysis
aligned over the forefoot. Terminal stance (31–50% of the gait cycle) be-
gins with heel rise and continues until the contralateral foot strikes the The normal distribution of the present sample was confirmed using
ground. To determine the foot progression angle, the angle of the long the Kolmogorov–Smirnov test. Means and standard deviations of the
axis of the foot segment in the global (lab) coordinate system relative variables of interest were calculated. Simple linear regression (Pearson
to the walking directions axis was computed. product–moment correlation coefficient; r) was used to examine the
association between static varus malalignment and gait parameters as
2.3. Radiographic methods well as between the MAA measured from standing radiographs and
the static lower limb alignment measurements in the frontal plane
Radiographic assessment of lower limb alignment was conducted on based on reflective markers. The significance level adopted in this
the same day as the gait analysis. Patients stood barefoot in a forward study was set at p b 0.05. We interpreted correlation values below
knee position with the patella centered over the femoral condyles and 0.30 as low, between 0.30 and 0.65 as medium, and correlations above
feet straight ahead to control for any foot rotation effects [24] and to at- 0.65 as high [27]. Differences between groups were tested for signifi-
tain a true full-length weight bearing anteroposterior radiograph [25]. cance using a Student's t-test. The statistical calculations were carried
On each radiograph, the joint centers of the hip, knee, and ankle were out using the SPSS version 18.0.0 (Chicago, IL, USA). Post hoc power
identified. In accordance with Miyazaki et al. [4], Hunt et al. [7], and calculations were determined with the analysis software R (package
Mündermann et al. [8] using the same method for a similar purpose, pwr, version 1.1.1) and according to Cohen [27].
the MAA of the lower extremity was used to quantify alignment in the
frontal plane and obtained with the analysis software DiagnostiX-32 3. Results
(Gemed) by the same investigator. Alignment was measured as the
angle formed by the line from the femoral head center to the femoral Subject group characteristics are summarized in Table 1. No significant differences
were observed across groups for self-selected walking speed, passive hip rotation, passive
intercondylar notch center and the line from the ankle talus center to tibial torsion and anthropometric parameters.
the center of the tibial spine tips. In accordance with the study of Post hoc power calculations revealed that a sample size of 18 patients provides 80%
Specogna et al. [26], reliability of MAA measurements was high (ICC power for detecting a correlation coefficient between the MAA and frontal/transverse
= 0.97). The MAA measured from standing radiographs uses therefore plane kinematic and kinetic parameters as small as r = 0.62 (p = 0.05, two sided).
Fig. 2 shows a strong linear relationship (r = 0.834, p b 0.001, power = 100%) between
the same landmarks and definitions like the marker-based three-
the MAA measured from standing radiographs and the static lower limb alignment mea-
dimensional gait analysis to measure lower limb alignment in the surements in the frontal plane based on reflective markers and the gait analysis system.
Linear correlations between the MAA measured from standing radiographs and gait pa-
rameters in the transverse plane are presented in Table 2. High correlations with increased
Table 2
internal knee rotation (tibia rotation; r = 0.696, p = 0.004, power = 88%) and medium cor-
Correlation coefficients (r) to static mechanical axis angle and correlation p-values for
relations with increased endorotation of the foot (internal foot placement; r = 0.584, p =
transverse plane kinematic and kinetic parameters during stance phase in the patient
0.022, power = 74%) during the stance phase of gait were detected. Regarding the kinetic
group (n = 18).
data, significant, high linear correlations with the static MAA are shown for the maximum in-
Joint Parameter r p-value ternal knee rotation moment in terminal stance (r = 0.660, p = 0.007, power = 87%) and
the maximum external hip rotation moment in loading response/mid stance (r = −0.661,
Angles (°) p = 0.007, power = 87%).
Foot Max. endorotation stance phase 0.584 0.022 Furthermore, the maximum external knee adduction moment in terminal stance
Knee Max. internal rotation terminal stance 0.696 0.004 was linearly correlated with maximum internal knee rotation (r = 0.823, p b 0.001,
Hip Max. internal rotation stance phase −0.459 0.085 power = 94%) in terminal stance and maximum internal hip rotation during stance
phase (r = −0.742, p = 0.002, power = 90%).
Moments (nm/kg)
Differences between the patient and control groups are shown in Fig. 3. Patients with
Knee Max. internal rotation terminal stance 0.660 0.007
varus malalignment of the knee were walking with a significantly increased endorotation
Hip Max. external rotation loading response/mid stance −0.661 0.007
of the foot compared to healthy controls. A post hoc power calculation revealed that the
Max. internal rotation terminal stance 0.040 0.886
difference in maximum foot endorotation between our study groups (18 patients, 15
Internal rotation is positive; external rotation is negative. controls) has a power of 95%.
F. Stief et al. / The Knee 21 (2014) 688–693 691

20.0

17.5

15.0
MAA, radiograph [°]

12.5

10.0

7.5

5.0

2.5

2.5 5.0 7.5 10.0 12.5 15.0 17.5 20.0

Lower limb alignment in the frontal plane, reflective markers [°]

Fig. 2. Scatter diagram of the relationship between the radiographic mechanical axis angle (MAA) and the static lower limb alignment measurements in the frontal plane based on reflec-
tive markers and the gait analysis system (r = 0.834, p b 0.001, power = 100%) for patients with varus malalignment of the knee (n = 18).

4. Discussion transverse plane rotations during gait may either be a potential gait
mechanism to compensate for excessive varus malalignment of the
The primary objective of the present study was to investigate the knee or essential in response to the altered MAA. As a result, this mod-
correlation between static varus malalignment of the knee and dynamic ified gait pattern in patients with varus malalignment may explain the
measures of the lower extremity during gait in the transverse plane. The increased internal knee rotation moments compared to normally
results suggest that a linear association exists between lower extremity aligned controls in a previous study [13]. Astephen et al. [28] also re-
varus malalignment and an increased endorotation of the foot as well as ported a greater knee internal rotation moment coupled with a net
an increased maximum internal knee rotation (tibia rotation). Patients hip external rotation moment in patients with knee OA compared to a
with varus malalignment of the knee showed a significantly increased healthy control group.
internal foot placement (9.0°) during stance phase compared to the Regarding the accuracy of three-dimensional gait parameters, the
control subjects without varus malalignment (1.3°), which could be strong linear relationship between the MAA (radiologically) and the
caused by the tendential increased tibia rotation in the patient group MAA (based on reflective markers) suggests the suitability of the used
(7.9°) compared to the control group (3.7°). Due to the fact that the marker-based lower body protocol to analyze patients with varus
passive hip rotation and passive tibial torsion were not significantly malalignment of the knee. No significant differences were observed
different between groups (Table 1), the observed differences in between patients and controls for self-selected walking speed. Thus,

Foot Endorotation Knee Internal Rotation Hip Internal Rotation


Stance Phase Terminal Stance Stance Phase
30
p = 0.854
p = 0.306
25

20 p = 0.003
13.6 14.1
15
Angle [°]

9.0 7.9
10
3.7
5
1.3
0

-5

-10
Patients (n = 18) Controls (n = 15)

Fig. 3. Average values with standard deviation for maximum foot, knee and hip angles during stance phase in the transverse plane.
692 F. Stief et al. / The Knee 21 (2014) 688–693

differences in gait patterns could not be attributed to differences in In conclusion, the results of the present study indicated that biome-
walking speed. chanical changes in the transverse plane occur concomitantly with
The external knee adduction moment was linearly correlated with in- changes in knee malalignment in the frontal plane independent from
ternal knee (positive correlation) and hip rotation (negative correlation) the presence of knee OA. A mechanical consequence of varus knee
during the stance phase. This suggests that transverse plane gait me- malalignment is obviously an internal foot placement and an internal
chanics in patients with varus malalignment of the knee but no signs of knee rotation in conjunction with an increase of the internal knee rota-
knee OA are directly in conjunction with the external knee adduction tion moment and external knee adduction moment during the stance
moment which is a contributing factor to articular cartilage degeneration phase of gait. Therefore, varus malalignment of the knee should not be
and disease progression in the medial knee compartment [4,5,9,10] (sec- viewed as an isolated problem in the frontal plane.
ond part of the hypothesis). This assumption is confirmed with the stud-
ies of Davids et al. [29] and MacWilliams et al. [30] that demonstrated
Conflict of interest statement
that an increased knee rotation in children with symptomatic intoeing
gait leads to an increased knee adduction moment in the coronal plane
The authors disclose any financial and personal relationships with
during the stance phase of gait. These findings lead to the conclusion
other people or organizations that could inappropriately influence
that transverse plane bone morphology is associated with coronal knee
their work.
loading during gait, which may have important implications for the pro-
gression of OA in this patient group. It has been suggested that changes in
transverse plane mechanics at the knee can initiate degenerative chang- References
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