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Gait & Posture 36 (2012) 276–281

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Gait & Posture


journal homepage: www.elsevier.com/locate/gaitpost

The relative contributions of the prosthetic and sound limb to balance control
in unilateral transtibial amputees
Carolin Curtze a,*, At L. Hof a,b, Klaas Postema a, Bert Otten b
a
Department of Rehabilitation Medicine, Center for Rehabilitation, University Medical Center Groningen, Groningen, The Netherlands
b
Center for Human Movement Sciences, University of Groningen, Groningen, The Netherlands

A R T I C L E I N F O A B S T R A C T

Article history: In unilateral transtibial amputees maintenance of standing balance is compromised due to the lack of
Received 17 April 2011 active ankle control in the prosthetic limb. The purpose of this study is to disentangle the contribution of
Received in revised form 24 November 2011 the prosthetic and sound limb to balance control following waist-pull perturbations. We compared the
Accepted 7 March 2012
contribution of the hip and ankle joints to balance control of 15 unilateral transtibial amputees and 13
able-bodied controls after been externally perturbed through release of a pulling force. Perturbations
Keywords: were applied in four different directions. Outcome measure was the proportion of joint moment
Amputee
integrated over time generated by the hip and ankle joints in order to restore static stability after
Balance
perturbation. Analyses revealed that perturbations in backward/forward direction were recovered
Perturbation
Ankle mainly by the ankle strategy. The amputees compensated for the absence of active ankle control in the
Hip prosthetic limb by increasing the ankle moment in the sound limb. Interestingly, the passive properties
Moment of the prosthetic foot contributed to balance control, which has important implications for prosthetic
Joint moment integral fitting and standing stability in lower limb amputees. Amputees and controls resisted perturbations in
medio-lateral direction by generating the necessary hip moments. Finally, these findings are discussed
with respect to prosthetic design and rehabilitation processes.
ß 2012 Elsevier B.V. All rights reserved.

1. Introduction The direction of FG can be modulated by generating a hip


moment (MH), thereby moving the CoM. In so doing, a horizontal
While standing in highly frequented places, we oftentimes force (FHM) is produced
are subject to perturbations caused by others inadvertently
coming into contact with us. Here, balance is threatened as
perturbations applied to the upper body will accelerate the MH
F HM ¼
body’s center of mass (CoM) toward the boundary of the base of L
support. In order to withstand these perturbations without in which L is the leg length, i.e. the trochantic height.
losing balance, we can use different balance control strategies. In the ankle strategy, the position of the CoP under the feet is
Depending on the magnitude of the external perturbation, moved by means of muscles action around the ankle joint. When
balance can be restored by means of the ankle and/or hip only the ankle moment (MA) is acting the horizontal component
strategy, or the load–unload strategy [1]; large perturbations (FAM) of FG is
will require a protective stepping strategy [2]. When standing in
perfect equilibrium the CoM is vertically above the center of
pressure (CoP), and the ground reaction force (FG) is pointing MA
F AM ¼
toward the CoM (Fig. 1). After being perturbed by a horizontal H
force, such as a push or pull, it is important to generate an in which H is the height of the CoM.
equivalent force in opposite direction; this can either be done by To compare the amount of ankle and hip strategy used, it will be
the hip or the ankle strategy or a combination of both strategies. assumed that H  L, which is approximately true for most humans.
With this approximation the horizontal component of FG due to hip
or ankle FHM and FAM are both proportional to the joint moments
MH and MA. This allows a simple comparison of the amount of ankle
* Corresponding author at: Department of Rehabilitation Medicine, Center for
Rehabilitation, University Medical Center Groningen, P.O. Box 30.001, 9700 RB
and hip strategy used.
Groningen, The Netherlands. Fax: +31 50 3619251. Note that Fig. 1 and the principle outlined above are based on
E-mail address: c.curtze@umcg.nl (C. Curtze). the choice of the position of the ankle and hip joints being aligned

0966-6362/$ – see front matter ß 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2012.03.010
C. Curtze et al. / Gait & Posture 36 (2012) 276–281 277

interesting as these individuals lack the active control of the


Nomenclature
prosthetic ankle joint, while having two intact hip joints and one
intact ankle joint. In this task, when standing with extended knees,
FG ground reaction force (Nm) the knee joints do not contribute to balance control. The aim of this
FHM horizontal component of FG generated by MH study is to disentangle the contribution of the prosthetic and sound
FAM horizontal component of FG generated by MA limb/joints to balance control. We hypothesised that unilateral
L leg length (trochanteric height) transtibial amputees compensate for the lack of active ankle
H height of CoM control in the prosthetic limb by increasing the contribution of the
MA ankle moment sound limb to balance control [7]. A study on the corrective ankle
MH hip moment moments in lower limb amputees in response to platform
perturbations revealed that the stiffness of the prosthetic ankle
CoP center of pressure
contributes to balance control [13]. Perturbations in the sagittal
CoM center of mass
plane were expected to result in an increase of ankle moment in
MAS normalized ankle moment of the sound limb (Nm/ the sound limb compared to the prosthetic limb or an able-bodied
kg) limb. No differences in the contribution of the prosthetic and sound
MAP normalized ankle moment of the prosthetic limb limb were expected for perturbations in the frontal plane, as the
(Nm/kg) load–unload strategy is acting and the hip joints of transtibial
MHS normalized hip moment of the sound limb (Nm/kg) amputees are muscle empowered, just like in able-bodied controls.
MHP normalized hip moment of the prosthetic limb A better understanding of the dynamics of balance control will help
(Nm/kg) to improve prosthetic design and rehabilitation processes.
Msum sum of normalized moments (MAS + MAP +
MHS + MHP) (Nm/kg) 2. Methods

2.1. Simulation
with the ground reaction force. This in reality is usually not the
case (for instance the CoP is often in front of the ankle joint), but the To validate the above mentioned assumption of H  L, a
principle of horizontal force changes still holds when offset simulation of a simple planar mechanism of two elements
moments of force are required for static standing. constrained by an endpoint is performed [14]. The elements are
Pioneering work by Horak and Nashner [12] has shown a connected to each other with a hinge joint. The human body
dominance of the ankle strategy during small perturbations such modeled is a person of 1.80 m tall and 80 kg body weight. The mass
as brief horizontal platform translations in anterior–posterior and length data of the head, arms, and trunk (HAT) segment and
direction. In the medio-lateral direction the position of the CoP is the leg segment were based on Winter [15]. It turns out that a hip
controlled by the hip abductors/adductors working in antiphase, moment of 100 Nm produces 162 N horizontal FG. Applying a
i.e. the load–unload strategy. During quiet standing the hip moment of the same magnitude at the ankle produces 129 N
abductors/adductors moments are equal in magnitude, so that horizontal FG. The separate contributions add up to a combined
their effects cancel [1]. effect of 291 N horizontal FG. The hip moment contributes 55% and
For lower limb amputees external perturbations are particu- the ankle moment 45% of the total horizontal FG at equal joint
larly challenging, as their balance is impaired due to the absence of moments. Sensitivity analysis revealed that these relative con-
active muscular control of one or more joints. An approach to study tributions of the hip and ankle joints were robust against changes
the effect of external perturbations on quiet standing is to apply in hip joint location.
sudden pulls to the waist [3–6]. In previous research this task has
been used in able-bodied subjects to investigate the boundaries of 2.2. Experimental
protective stepping as a response to sudden waist-pull perturba-
tions [3–5]. In the present study only mild perturbations will be 2.2.1. Participants
applied which can be withstood without stepping. Studying the Fifteen male unilateral transtibial amputees and 13 able-bodied
response of unilateral transtibial amputees appears particularly controls were included in the study. The amputees had a mean age

Fig. 1. Hip and ankle strategy. Quiet standing in perfect equilibrium versus (A) hip strategy and (B) ankle strategy.
278 C. Curtze et al. / Gait & Posture 36 (2012) 276–281

Fig. 2. Experimental setup. The participant resists a force pulling from the left. The electromagnet was used as release mechanism. Through release of the load a fall was
induced opposite to direction the pulling load. The reading of the force transducer was used to determine the moment of release of the load. The participant was positioned on
two force plates. The setup was equivalent for all four perturbation conditions.

of 55.1  9.8 years, height of 1.83  0.52 m and weight beforehand. The lateral distance between the medial edges of the
92.5  13.9 kg. Reasons for amputation were trauma (10), vascular feet was set to 20% the height of application of the pulling force,
disease (4), and limb deficiency (1). Five of the 15 amputees had which is about hip width. The participant was verbally instructed
undergone an amputation of their right limb. The median time since to resist the perturbation, without performing a step. The
amputation was 7 years (range 2–44 years). All amputees were participants were secured by a safety harness system. The study
experienced and able walkers. In the experiment the amputees used was approved by the local Medical Ethical Committee.
their habitual prostheses which were equipped with one of the
following prosthetic feet: Otto Bock: 1C40 (7), 1D10 (3), 1D35 (2), 2.2.4. Data analysis
1A30 (2), and Endolite: Multiflex (1). The controls had a mean age of The moment of release (t0) was determined by means of
53.1  10.6 years, height of 1.87  0.56 m and weight of readings from the force transducer. The return of static stability/
87.2  10.1 kg. balance (t1) was defined as the moment at which the ground
reaction force component in the direction of pull remains within
2.2.2. Apparatus 1 SD of the mean of static stability/balance, i.e. quiet standing
The ground reaction forces were measured by two force plates, without the load applied.
sampled at a rate of 1000 Hz (Fig. 2). The kinematics were tracked Finally, to disentangle the contribution of prosthetic and sound
by an eight-camera Vicon motion capture system sampled at a rate limb to balance control, the hip and ankle moment of each of both
of 100 Hz. A total of 35 reflective markers were placed on limbs were determined in the direction of perturbation. In the
anatomical landmarks as specified in the Vicon Plug-in Gait full- anterior–posterior perturbation condition, an increase in moment
body model. Markers placed on the prosthetic limb matched the indicates plantar/hip flexion. In the medio-lateral perturbation
marker positions on the sound limb. Finally, anthropometric conditions an increase in moment in the limb ipsilateral to the fall
measurements were taken according to the requirements of the indicates ankle inversion/hip abduction, while in the limb
model, i.e. body mass, height, leg length (anterior superior iliac contralateral to the fall a decrease in moment indicates ankle
spine to medial malleolus), knee width (flexion axis), and ankle inversion/hip abduction. Note that the limbs have opposite signs
width (medial and lateral malleoli) for each of the limbs. for ankle inversion/hip abduction, as their effects cancel.
The setup for the perturbations consisted of a cable running Before determining the normalized joint moment integral
over a pulley which was attached to a force transducer. The load generated by each of the four joints, the time-series data of the
was connected to the cable by means of an electromagnet; with a normalized moments (Nm/kg) were shifted by their baseline value,
switch the load could be released. i.e. set to zero for t1. This value corresponds to the equilibrium
value for quiet standing without the load applied, which was used
2.2.3. Procedure as reference point. By numerically integrating the normalized
The participant stood upright with their feet parallel. Each foot moment over time (t0  t1), the normalized joint moment integral
was positioned on a separate force plate. A horizontal force was (Nm s/kg), was determined. Subsequently, the contribution of each
applied to his waist via a cable as described above (Fig. 2). The of the joints was expressed as a proportion of the total joint
participant was resisting the load before it was released by the moment integral of all four joints.
experimenter at an unpredictable moment, inducing a fall opposite
to the pulling direction. The participant had to compensate for that 2.2.5. Statistical analysis
perturbation. Falls were induced in four different directions: (A) For each of the perturbation conditions, the mean proportion of
backward, (B) forward, (C) toward the sound/right limb, and (D) joint moment integral was calculated for each of the four joints.
toward the prosthetic/left limb, by releasing a load pulling in The mean value was calculated from multiple trials from the same
opposite direction. The order of perturbations was randomized participant. Differences in outcome between the two groups were
over participants; three trials were performed per direction. The tested by one-way ANOVAs. Paired t-tests were used to compare
load was relative to the participant’s body weight: 2.5% in the contribution of the ankle/hip joint of the left/prosthetic and
anterior–posterior, and 5% in medio-lateral direction. The parti- right/sound limb to balance control. The significance level was set
cipant’s body weight (including the prosthesis) was determined to p  .05.
C. Curtze et al. / Gait & Posture 36 (2012) 276–281 279

backward induced fall forward induced fall


0.6 0.6

A B
0.4 0.4
moment (Nm/kg)

moment (Nm/kg)
0.2 0.2

0 0

−0.2 MAS −0.2 MAS


MAP MAP
−0.4 −0.4
MHS MHS
MHP MHP
−0.6 −0.6
Msum M
sum

−0.8 −0.8
−1 −0.5 0 0.5 1 1.5 2 2.5 3 −1 −0.5 0 0.5 1 1.5 2 2.5 3
time (s) time (s)

fall induced towards sound limb fall induced towards prosthetic limb
0.4 0.4
MAS
0.3
C MAP 0.3
D
M
HS
0.2 M 0.2
moment (Nm/kg)

moment (Nm/kg)
HP
M
sum
0.1 0.1

0 0

−0.1 −0.1 M
AS
MAP
−0.2 −0.2
MHS

−0.3 −0.3 MHP


Msum
−0.4 −0.4
−1 −0.5 0 0.5 1 1.5 2 2.5 3 −1 −0.5 0 0.5 1 1.5 2 2.5 3
time (s) time (s)

Fig. 3. Normalized ankle and hip moments in the direction of perturbation as a function of time. Exemplary normalized ankle moments of the sound (MAS) and prosthetic (MAP)
limb, normalized hip moments of the sound (MHS) and prosthetic (MHP) limb, and the sum of the normalized moments (Msum) are given for a single amputee participant. A fall
was induced (A) backward, (B) forward, (C) toward the sound limb, and (D) toward the prosthetic limb by releasing a load that was pulling in opposite direction. At t0 the load
was released, static balance was restored at t1. All moments are set to zero for t1. In (A and B) an increase in moment indicates plantar flexion/hip flexion. In (C and D) an
increase in moment in the limb ipsilateral to the fall indicates ankle inversion/hip abduction, while in the limb contralateral to the fall a decrease in moment indicates ankle
inversion/hip abduction. Note that the limbs have opposite signs for ankle inversion/hip abduction, as their effects cancel.

3. Results was no difference in contribution between the hip of the prosthetic


(6%) and sound (4%) limb (t(14) = .223, p = .826). In the controls the
Exemplary time series data of the normalized ankle and hip right (41%) and left (45%) ankle contributed equally to balance
moments for all four perturbation conditions are shown in Fig. 3. control after a fall was induced in backward direction
The data are set to zero for t1, which allows a better comparison of (t(12) =  .845, p = .414). Furthermore, there was no significant
the contribution of each of the joints. In Fig. 3A, the amputee resists difference in contribution of the right (5%) and left (9%) hip
the forward pull by the load, which is released at t0. The sum of (t(12) =  .563, p = .584). The proportion of joint moment integral
normalized moments (Msum) reveals that it takes about 100– of the ankle (43%) was significantly higher than that of the hip (7%;
200 ms before the actual balance recovery response is initiated, i.e. t(12) = 11.143, p < .001), which shows that the controls used an
drop in Msum after release. In this short time window the ankle strategy to recover balance. Between-group comparison
participants starts to fall backwards. It is mainly the ankle revealed a significantly higher proportion of joint moment integral
moment generated by the sound limb (MAS) and the passive in the sound (53%) ankle of amputees than that in able-bodied
properties of the prosthetic ankle (MAP) that appear to contribute controls (43%; F(1,26) = 4.806, p = .038).
to balance recovery, while the hip moments of the sound (MHS) and The induced forward fall depicted in Fig. 3B shows the
prosthetic (MHP) limb seem to contribute less. In the late phase of comparable pattern as for the backward fall, but in direction
balance recovery, about 1.5 s after the release of the load, there is a reversed. In the initial phase, before release of the load, the amputee
small overshoot of Msum, before the amputee is in static balance at is resisting the backward pull of the load by means of the ankle
t1. Note that Msum is not the total moment of force acting on the moment generated by the sound limb. In this case, the prosthetic
body, but the sum of the moments of the separate joints is directly (11%) ankle appears to contribute less to balance recovery
related with the balance recovering ground reaction force evoked. (t(14) = 6.504, p < .001; Fig. 4B); the amputees were greatly relying
By determining the proportion of joint moment integral the on their sound ankle (69%). The controls, however, used their right
contribution of each joint to balance control can be dissociated. The (36%) and left (42%) ankle equally (t(12) =  .985, p = .344), and their
proportion of joint moment integral for the amputees and controls right (11%) and left (12%) hip joints equally as well (t(12) =  .167,
for each of the perturbation conditions is given in Fig. 4. In the p = .870). Further analysis revealed that the ankle strategy was
amputees the sound (53%) ankle contributed significantly more to predominant in the control group (t(12) = 10.813, p < .001). Marked
balance control after a fall induced in backward direction than the between-group differences were found for the proportion of joint
prosthetic (37%) ankle (t(14) = 2.197, p = .045; Fig. 4A), while there moment integral of the ankle. While the sound (69%) ankle of
280 C. Curtze et al. / Gait & Posture 36 (2012) 276–281

Fig. 4. Joint moment integrals as proportion of total for four different load release conditions: A fall was induced (A) backward, (B) forward, (C) toward the sound/right limb,
(D) toward the prosthetic/left limb, by releasing a load that was pulling in opposite direction. Error bars depict  1 SD.

amputees contributed significantly more to balance control than In the controls, the hip joint contralateral (63%) to the pulling
the ankle (39%) in able-bodied controls (F(1,26) = 23.672, p < .001), load contributed significantly more to balance recovery than the
the prosthetic (11%) ankle contributed significantly less proximal (37%) hip joint (t(12) = 4.233, p = .001; Fig. 4C and D). No
(F(1,26) = 25.627, p < .001). differences in proportion of joint moment integral were found for
In the medio-lateral perturbation conditions, Fig. 3C and D, the the ankle joints (t(12) =  .586, p = .569).
amputee achieved stable balance by means of the load–unload
strategy. Thus, balance is accomplished by the hip abductor/ 4. Discussion
adductor moments and virtually no contribution of the ankle joints.
In the early response, after release, the hip abduction moment in the In this study we disentangled the contribution of the prosthetic
limb proximal to the pulling load is reduced, while the hip abduction and sound limb to balance control in unilateral transtibial amputees
moment in the limb contralateral to the pulling load is increased following waist-pull perturbations. We found that perturbations in
before it finally converges toward its baseline value. the anterior–posterior direction are recovered by the ankle strategy,
When a sideward fall was induced to the sound limb, by while the hips play only a subordinate function, i.e. they contributed
releasing a load to the side of the prosthetic limb, the sound (61%) to a much lesser extent. In the induced backward fall condition the
hip joint contributed significantly more to balance recovery than passive properties of the prosthetic foot contributed significantly to
the hip joint of the prosthetic (37%) limb (t(14) = 3.145, p = .007; balance recovery in amputees; yet there was considerable
Fig. 4C). Furthermore, there was a significant difference in joint compensation by the ankle of the sound limb. Horak and Nashner
moment integral generated by the prosthetic (6%) and sound (4%) [12] demonstrated that healthy people, when being perturbed while
ankle joint (t(14) =  2.640, p = .019). When the fall was induced to standing on a support surface shorter than the foot length,
the prosthetic limb, by releasing a load to the opposite side, no compensate for the loss of ankle strategy by using the hip strategy.
significant difference was found with respect to the contribution of Yet, the amputees in our study preferred to increase the contribution
the hip joints of the sound (47%) and prosthetic (68%) limb of the sound limb. In the induced forward fall condition the sound
(t(14) =  1.734, p = .105; Fig. 4D). Moreover, there was no ankle compensated almost fully for the lack of active ankle moment
significant difference in contribution between the prosthetic in the prosthetic limb. This compensation effect agrees with the
(14%) and sound (1%) ankle joint (t(14) = 1.949, p = .072). control strategies used by unilateral lower limb amputees when
C. Curtze et al. / Gait & Posture 36 (2012) 276–281 281

balancing on a moving platform [7]. The results of this study showed the contribution of a prosthetic foot varies between models, this
that most adjustments strategies in amputees occurred in the sound should be considered in the prosthetic fitting process. To optimize
limb, under which they increased CoP movement and loading [7]. In the patient-prosthesis match, an amputee’s control and muscle
another platform perturbation study it was further shown that the strength in the intact hip and ankle joints and the amount of stability
contribution of both ankles to balance control was even more provided by the prosthetic device [11,13] should complement each
asymmetric than the asymmetry in loading [13]. Besides, the study other, for instance by applying balance measures [16].
confirmed the contribution of the passive ankle properties to
balance control in anterior–posterior direction [13]. The finding has Suppliers
important implications for prosthetic design and fitting. Zmitrewicz
et al. [8] have shown that a passive prosthetic foot-ankle device is  Advanced Mechanical Technology Inc., 176 Waltham Street,
functionally similar to the soleus muscle. Amputees with good Watertown, MA 02472-4800, USA.
muscle strength and control in the sound ankle can compensate for  Vicon Motion System, 14 Minus Business Park, West Way,
the lack of ankle strategy in the prosthetic limb. The ankle muscles Oxford, OX2OJB, UK.
are essential in recovering from a trip [9] and are the primary  Brosa AG, Dr. Klein Straße 1, 88069 Tettnang, Germany.
contributors to controlling whole-body sagittal plane angular  The MathWorks Inc., 3 Apple Hill Drive, Natick, MA 01760-2098,
momentum [10]. USA.
Less able amputees will profit from a prosthetic foot with a large  SPSS Inc., 233 S. Wacker Drive, 11th floor, Chicago, IL 60606-
radius of curvature to improve standing stability [11]. In the present 6307, USA.
study, the amputees wore their habitual prosthesis equipped with a
variety of different prosthetic feet. While the general response
Acknowledgments
patterns described in this article were strong, this variation in
prosthetic feet may have had an impact on an individual’s response
This work was supported by a non commercial grant of OIM
to the perturbations. In future research, it would be interesting to
Foundation, Assen, The Netherlands, and Stichting Beatrixoord
systematically manipulate the radius of curvature of the prosthetic
Noord-Nederland, The Netherlands. Furthermore, the authors
foot and test its effect on an individual’s balance response.
thank Ronald Davidsz for his assistance with the data collection.
To recover from perturbations in the medio-lateral direction,
amputees as well as controls used the load–unload mechanism, Conflict of interest statement
which is driven by modulation of the hip moments. In previous The authors declare to have no conflict of interest in this work.
research this has been shown to be the common balance strategy,
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