Gait in adolescent idiopathic scoliosis: Energy cost analysis

Article (PDF Available)inEuropean Spine Journal 18(8):1160-8 · May 2009with68 Reads
DOI: 10.1007/s00586-009-1002-0 · Source: PubMed
Abstract
Walking is a very common activity for the human body. It is so common that the musculoskeletal and cardiovascular systems are optimized to have the minimum energetic cost at 4 km/h (spontaneous speed). A previous study showed that lumbar and thoracolumbar adolescent idiopathic scoliosis (AIS) patients exhibit a reduction of shoulder, pelvic, and hip frontal mobility during gait. A longer contraction duration of the spinal and pelvic muscles was also noted. The energetic cost (C) of walking is normally linked to the actual mechanical work muscles have to perform. This total mechanical work (W(tot)) can be divided in two parts: the work needed to move the shoulders and lower limbs relative to the center of mass of the body (COM(b)) is known as the internal work (W(int)), whereas additional work, known as external work (W(ext)), is needed to accelerate and lift up the COM(b) relative to the ground. Normally, the COM(b) goes up and down by 3 cm with every step. Pathological walking usually leads to an increase in W (tot) (often because of increased vertical displacement of the COM(b)), and consequently, it increases the energetic cost. The goal of this study is to investigate the effects of scoliosis and scoliosis severity on the mechanical work and energetic cost of walking. Fifty-four female subjects aged 12 to 17 were used in this study. Thirteen healthy girls were in the control group, 12 were in scoliosis group 1 (Cobb angle [Cb] < or = 20 degrees), 13 were in scoliosis group 2 (20 degrees < Cb < 40 degrees), and 16 were in scoliosis group 3 (Cb > or = 40 degrees). They were assessed by physical examination and gait analysis. The 41 scoliotic patients had an untreated progressive left thoracolumbar or lumbar AIS. During gait analysis, the subject was asked to walk on a treadmill at 4 km h(-1). Movements of the limbs were followed by six infrared cameras, which tracked markers fixed on the body. W(int) was calculated from the kinematics. The movements of the COM(b) were derived from the ground reaction forces, and W(ext) was calculated from the force signal. W(tot) was equal to W(int) + W(ext). Oxygen consumption VO2 was measured with a mask to calculate energetic cost (C) and muscular efficiency (W(tot)/C). Statistical comparisons between the groups were performed using an analysis of variance (ANOVA). The external work (W(ext)) and internal work (W(int)) were both reduced from 7 to 22% as a function of the severity of the scoliosis curve. Overall, the total muscular mechanical work (W(tot)) was reduced from 7% to 13% in the scoliosis patients. Within scoliosis groups, the W(ext) for the group 1 (Cb > or = 20 degrees) and 2 (20 < or = Cb < or = 40 degrees) was significantly different from group 3 (Cb > or = 40 degrees). No significant differences were observed between scoliosis groups for the W(int). The W(tot) did not showed any significant difference between scoliosis groups except between group 1 and 3. The energy cost and VO2 were increased by around 30%. As a result Muscle efficiency was significantly decreased by 23% to 32%, but no significant differences related to the severity of the scoliosis were noted. This study shows that scoliosis patients have inefficient muscles during walking. Muscle efficiency was so severely decreased that it could be used as a diagnostic tool, since every scoliosis patient had an average muscle efficiency below 27%, whereas every control had an average muscle efficiency above 27%. The reduction of mechanical work found in scoliotic patients has never been observed in any pathological gait, but it is interpreted as a long term adaptation to economize energy and face poor muscle efficiency. With a relatively stiff gait, scoliosis patients also limit vertical movement of the COM(b) (smoothing the gait) and consequently, reduce W(ext) and W(int). Inefficiency of scoliosis muscles was obvious even in mild scoliosis (group 1, Cb < 20 degrees) and could be related to the prolonged muscle contraction time observed in a previous study (muscle co-contraction).
ORIGINAL ARTICLE
Gait in adolescent idiopathic scoliosis: energy cost analysis
P. Mahaudens Æ C. Detrembleur Æ M. Mousny Æ
X. Banse
Received: 14 October 2008 / Revised: 13 February 2009 / Accepted: 8 April 2009 / Published online: 24 April 2009
Ó Springer-Verlag 2009
Abstract Walking is a very common activity for the
human body. It is so common that the musculoskeletal and
cardiovascular systems are optimized to have the minimum
energetic cost at 4 km/h (spontaneous speed). A previous
study showed that lumbar and thoracolumbar adolescent
idiopathic scoliosis (AIS) patients exhibit a reduction of
shoulder, pelvic, and hip frontal mobility during gait. A
longer contraction duration of the spinal and pelvic muscles
was also noted. The energetic cost (C) of walking is normally
linked to the actual mechanical work muscles have to per-
form. This total mechanical work (W
tot
) can be divided in two
parts: the work needed to move the shoulders and lower
limbs relative to the center of mass of the body (COM
b
)is
known as the internal work (W
int
), whereas additional work,
known as external work (W
ext
), is needed to accelerate and
lift up the COM
b
relative to the ground. Normally, the COM
b
goes up and down by 3 cm with every step. Pathological
walking usually leads to an increase in W
tot
(often because of
increased vertical displacement of the COM
b
), and conse-
quently, it increases the energetic cost. The goal of this study
is to investigate the effects of scoliosis and scoliosis severity
on the mechanical work and energetic cost of walking. Fifty-
four female subjects aged 12 to 17 were used in this study.
Thirteen healthy girls were in the control group, 12 were in
scoliosis group 1 (Cobb angle [Cb] B 20°), 13 were in sco-
liosis group 2 (20°\ Cb \ 40°), and 16 were in scoliosis
group 3 (Cb C 40°). They were assessed by physical
examination and gait analysis. The 41 scoliotic patients had
an untreated progressive left thoracolumbar or lumbar AIS.
During gait analysis, the subject was asked to walk on a
treadmill at 4 km h
-1
. Movements of the limbs were fol-
lowed by six infrared cameras, which tracked markers fixed
on the body. W
int
was calculated from the kinematics. The
movements of the COM
b
were derived from the ground
reaction forces, and W
ext
was calculated from the force sig-
nal. W
tot
was equal to W
int
? W
ext
. Oxygen consumption
_
VO
2

was measured with a mask to calculate energetic cost
(C) and muscular efficiency (W
tot
/C). Statistical comparisons
between the groups were performed using an analysis of
variance (ANOVA). The external work (W
ext
) and internal
work (W
int
) were both reduced from 7 to 22% as a function of
the severity of the scoliosis curve. Overall, the total muscular
mechanical work (W
tot
) was reduced from 7% to 13% in the
scoliosis patients. Within scoliosis groups, the W
ext
for the
group 1 (Cb C 20°) and 2 (20 B Cb B 40°) was signifi-
cantly different from group 3 (Cb C 40°). No significant
differences were observed between scoliosis groups for the
W
int
.TheW
tot
did not showed any significant difference
between scoliosis groups except between group 1 and 3. The
energy cost and
_
VO
2
were increased by around 30%. As a
result Muscle efficiency was significantly decreased by 23%
to 32%, but no significant differences related to the severity
P. Mahaudens (&)
Rehabilitation and Physical Medicine Unit,
Unite
´
de Re
´
adaptation, Universite
´
catholique de Louvain,
Tour Pasteur 5375, Avenue Mounier 53, 1200 Brussels, Belgium
e-mail: Philippe.Mahaudens@uclouvain.be
P. Mahaudens C. Detrembleur
Department of Physical Medicine and Rehabilitation,
Unite
´
de Re
´
adaptation, Universite
´
catholique de Louvain,
Tour Pasteur 5375, Avenue Mounier 53, 1200 Brussels, Belgium
M. Mousny X. Banse
Orthopaedic Research Laboratory, Universite
´
catholique
de Louvain, Tour Pasteur 9388, Avenue Mounier 53,
1200 Brussels, Belgium
P. Mahaudens
Orthopaedic Research Laboratory, Unite
´
de Re
´
adaptation,
Universite
´
catholique de Louvain, Tour Pasteur 5375,
Avenue Mounier 53, 1200 Brussels, Belgium
123
Eur Spine J (2009) 18:1160–1168
DOI 10.1007/s00586-009-1002-0
of the scoliosis were noted. This study shows that scoliosis
patients have inefficient muscles during walking. Muscle
efficiency was so severely decreased that it could be used as a
diagnostic tool, since every scoliosis patient had an average
muscle efficiency below 27%, whereas every control had an
average muscle efficiency above 27%. The reduction of
mechanical work found in scoliotic patients has never been
observed in any pathological gait, but it is interpreted as a long
term adaptation to economize energy and face poor muscle
efficiency. With a relatively stiff gait, scoliosis patients also
limit vertical movement of the COM
b
(smoothing the gait) and
consequently, reduce W
ext
and W
int
. Inefficiency of scoliosis
muscles was obvious even in mild scoliosis (group 1,
Cb \ 20°) and could be related to the prolonged muscle
contraction time observed in a previous study (muscle co-
contraction).
Keywords Scoliosis Gait Energy cost Pronostic
Introduction
Human walking is an essential daily activity that requires
correct joint mobilities and appropriate muscular force to
move the body. Both of these parameters engage mechanical
work [35] and energy expenditure, which are optimized in
normal walking at a spontaneous speed in order to minimize
the cost of locomotion [2, 24, 34].
Our previous study focused on changes in gait kine-
matics between thoraco-lumbar and lumbar Adolescent
Idiopathic Scoliosis (AIS) patients and healthy subjects
[21]. AIS patients have little reduction in trunk, pelvis, and
hip frontal mobility. Surprising, we also noticed a much
longer contraction duration of the bilateral lumbar and
pelvic muscles (rising from 30% to 50% of the gait cycle).
This increase in electrical activity was noticed even for
mild scoliosis (Cobb angle [Cb] \ 20°).
During walking, human beings not only move their lower
legs and pelvis, but also raise and lower their center of body
mass (COM
b
) at each step. Pelvic and hip frontal motion are
major determinants that serve to minimize and smooth the
vertical displacement of the COM
b
[9], allowing optimal
oxygen consumption during walking [16]. Disturbances of
the vertical displacement of the COM
b
in normal conditions
(e.g., walking on sand or carrying loads as an African
woman) [6, 18] or conditions of pathologic gait (e.g., stiff-
knee gait after a stroke or walking with a prosthesis) [10, 12,
27, 28] affect the mechanical work and metabolic cost of the
gait [1013, 18, 22, 27, 29, 30, 33]. More precisely, any
handicap increases these two parameters [10, 27, 29, 30, 33,
34]. Both muscular mechanical work, which is assessed by
the production of mechanical energy due to the energy
changes of the COM
b
relative to the ground and of the body
segments relative to the COM
b
[4, 5], and the energy
expenditure due to the oxygen consumption [32, 34]allow
assessment of the efficiency of locomotion. This efficiency is
underlined by a locomotor mechanism that can be compared
to an inverted pendulum (i.e., a pendulum-like mechanism).
At each stride, the COM
b
is successively behind or in front of
the point of contact with the foot on the ground. It thereby
produces gravitational potential and kinetic energy that are
continuously converted into one another like a pendulum, and
the resulting muscular mechanical work (W
tot
)requires
energy expenditure during walking. This energy expenditure
may be measured by the classical indirect calorimetric
method that remains the most reliable and practical method
based on the rate of O
2
consumption
_
VO
2

[25]. From this
measure, the physiological work (i.e., the energy per unit
distance travelled, also called energy cost or C) may be
computed. By comparing the energy cost of walking in
patients and healthy subjects, it is possible to evaluate the
energetic penalty of gait disability [34]. At a constant speed,
an increased energy cost means that the rate of O
2
con-
sumption increases and level of physical effort elevates. For
example, there is a progressive rise in the rate of energy
expenditure and a doubling of energy cost between normal
walking (4 km h
-1
) and running (8 km h
-1
)[15].
The problem occurs when the rate of O
2
consumption
_
VO
2

approaches its maximum
_
VO
2
max

; at this moment,
the consumption of oxygen is levelling off as anaerobic oxi-
dation processes occur. These processes result in the accu-
mulation of serum lactate and rapid muscular intolerance to
acidosis. Expressedas a percentageof the
_
VO
2
max,the rate of
oxygen consumption at a normal speed (4 km h
-1
)requires
approximately 20% of the
_
VO
2
max of an untrained normal
teen or young adult. The fact that walking taxes less than 50%
of the
_
VO
2
max in normal subjects and does not require
anaerobic activity accounts for the perception that walking
requires little effort in healthy individuals [34]. Indeed, an
excessive energy cost reduces the possibility of engaging in
activities and participating in social events.
By studying this variable in AIS, it is possible to gain
further insight into the mechanisms of pathological walk-
ing. The first goal of this study is to evaluate how light gait
changes observed in AIS patients affect the mechanical
work and energy expenditure during locomotion. The
second goal is to determine whether the severity of scolio-
sis curves influence these parameters.
Materials and methods
Study population
Fifty-four female subjects (13 healthy subjects and 41
untreated progressive AIS patients with comparable height,
Eur Spine J (2009) 18:1160–1168 1161
123
weight and body mass index) aged 12 to 17 years were
included in the study. The scoliosis patient group had a left
thoracolumbar or lumbar main structural curve (types 5 and 6
according to the Lenke classification [19]) and was divided in
three subgroups according to the Cobb angle (Cb) range:
group 1: Cb B 20° (n = 12), group 2: 20°\ Cb \ 40°
(n = 13), and group 3: Cb C 40° (n = 16) [7]. Girls under-
went a complete physical examination to detectanylocomotor
disorders, neurological abnormalities, and previous spinal
treatment or gait assessment. Scoliosis patients were submit-
ted to a radiological examination. Anthropometric and
radiological data are summarized in our previous study [21].
Every subject signed up for and participated freely in the
study, which was approved by the local ethics board.
Instrumented gait analysis
Gait was assessed by a three-dimensional analysis, which
included synchronous mechanical and energetic measure-
ments (Fig. 1).
The mechanical work was computed as follows: the total
positive mechanical work (W
tot
) done by the muscles dur-
ing walking was divided into the external work (W
ext
)
performed to move the COM
b
relative to the surroundings
and the internal work (W
int
) performed to move the body
segments relative to the COM
b
[35] (Fig. 2).
The external work (W
ext
) performed by the muscles to
accelerate and lift the COM
b
was computed from four force
transducers located at the four corners of the treadmill.
These transducers measured the 3D-ground reaction forces
according to Cavagna [3].
The three-dimensional accelerations (a) of the COM
b
were computed from the vertical (Fv), lateral (Fl), and
forward (Ff) components of the ground reaction forces (F)
and mass (m) of the subject (F=ma). The mathematical
integration of the three-dimensional accelerations gave the
velocity changes of the COM
b
in all three directions (V
v
,
V
l
, V
f
). From the instantaneous V
v
, V
l
, and V
f
and the body
mass (m), we computed the instantaneous kinetic energies
(E
k
= 1/2mV
2
) of the COM
b
(E
kv
, E
kl
, E
kf
). A second
mathematical integration of V
v
was performed to determine
the vertical COM
b
displacement (S
v
) and computed the
instantaneous gravitational potential energy (E
p
= mgS
v
).
The total external mechanical energy (E
tot
) of the COM
b
was calculated as the sum of the kinetic and potential
energies. The increments of the E
kv
, E
kl
, E
kf,
and E
p
curves
represented the positive work (W
ekv
, W
ekl
, W
ekf
, and W
ep
,
respectively) necessary to accelerate the COM
b
in the three
directions and lift the COM
b
during a stride. W
ext
was
obtained by summing the increments of E
tot
over a stride.
W
ekv
, W
ekl
, W
ekf
, W
ep,
and W
ext
were expressed in Joules
per kilogram body mass and per distance travelled.
The ‘Recovery’, quantifying the percent of mechanical
energy saved by a pendulum-like exchange between the
gravitational potential energy and kinetic energy of the COM
b
(i.e., an index reflecting the effectiveness of the pendulum-like
mechanical mode of walking) was calculated using the
following equation [3, 5]:
Recovery %ðÞ¼100
W
ek
jj
þ W
ep
W
ext
jj
W
ek
jj
þ W
ep
In this equation, W
ek
= W
ekf
? W
ekv
? W
ekl
and each
parameter was calculated as the sum of the positive
increments from the corresponding E
k,
E
p,
and E
tot
curves
(Fig. 2).
W
ek
? W
ep
is the maximum positive work (W
ext
) that
should be done without energy shift and represents the
work actually done [5].
The internal work (W
int
, the work required to move the
limbs relative to the COM
b
) was computed from kinematic
data following the method described by Willems et al. [35]
and Detrembleur et al. [12]. The body was divided into
Fig. 1 Energetic and
mechanical measurements.
Illustration of energy
expenditure (oxygen
consumption and energy cost)
measured by the classical
indirect calorimetric method
and mechanical work assessed
by the three-dimensional ground
reaction force
1162 Eur Spine J (2009) 18:1160–1168
123
seven rigid segments: head-arm-trunk (HAT), thighs,
shanks, and feet. The internal mechanical energy of the
body segments corresponded to the sum of the rotational
and translational energies of these segments due to their
movements relative to the COM
b
. For each lower limb, the
internal mechanical energy–time curves of the thigh,
shank, and foot were summed. The W
int
of each lower limb
and HAT segment was then calculated separately as the
Fig. 2 Evolution of external and internal mechanical energy as
function of time during gait at 4 km h
-1
. The upper figure represents
the curves of external energy (expressed in joules per kilogram body
mass and per meter travelled) as a function of time. These curves were
used to compute the external work (W
ext
) performed by the muscles to
accelerate and lift the COM
b
. The E
kf
curve represents the kinetic
energy variations linked to the speed of COM
b
displacement in the
forward direction. The E
v
curve represents the gravitational potential
(E
p
) and kinetic energy variations (E
kv
) linked to the speed of COM
b
displacement in the vertical direction. The E
kl
curve represents the
kinetic energy variations linked to the speed of COM
b
displacement in
the lateral direction. The total external mechanical energy (E
tot
) of the
COM
b
was calculated as the sum of the kinetic and potential energies.
The increments of E
kf
, E
v
, and E
kl
, curves represented the positive
work (W
ekf
, W
ev
and W
ekf
, respectively) necessary to accelerate the
COM
b
in the three directions and lift the COM
b
during a stride. W
ext
was obtained by summing the increments of E
tot
over a stride. The a
0
and b
0
vertical arrows show the increments of the external mechanical
energy curves measured on a healthy subject and an AIS patient with
Cb C 40°. The lower figure represents the curves of internal energy as
a function of time. These curves were used to compute the internal
work (W
int
) required to move the limbs relative to the COM
b
for the
head-arm-trunk (HAT) segment (Ei,
HAT
) as well as the left and right
lower limb segments (Ei,
LLL
and Ei,
RLL
). When the curves increase,
the muscles provide positive work to accelerate the body segments
relative to the COM
b
. The W
int
during gait corresponded to the sum of
the W
int
done to move the lower limbs and HAT segments, and it was
expressed in joules per kilogram body mass and per meter travelled.
The a, b, c, d, e, and f vertical arrows show the increments of the
internal mechanical energy curves
Eur Spine J (2009) 18:1160–1168 1163
123
sum of the increments of the respective internal mechanical
energy curves. Finally, W
int
during gait corresponded to the
sum of the W
int
done to move the lower limbs and HAT
segments and was expressed in joules per kilogram body
mass and per meter travelled.
The metabolic cost of walking was determined by the
subject’s oxygen consumption
_
VO
2

and carbon dioxide
production
_
VCO
2

; which were measured throughout the
treadmill test with an ergospirometer (Quark b
2
, Cosmed,
Italy) and expressed in ml kg
-1
min
-1
. The mass-specific
gross energy consumption rate (W kg
-1
) was obtained from
the oxygen consumption rate using an energy equivalent of
oxygen, taking into account the measured respiratory
exchange ratio (RER) [23]. The RER, computed as the ratio
between
_
VCO
2
and
_
VO
2
; always remained less than 1. Each
energy measurement started with a rest period in which the
subject was standing on the treadmill. Thereafter, they
walked until a steady state was reached and maintained for at
least 2 min. The Joules of energy expended per liter of
oxygen consumed were computed depending on the RER
according to the Lusk equation [23]. The energy expended
above the resting value (standing subtracted from walking
consumption) was divided by the walking speed (4 km h
-1
)
to obtain the net energy cost of walking (C,Jkg
-1
m
-1
)[4].
The efficiency (g) of positive work production by the muscles
was calculated as the ratio between W
tot
and C [4].
Protocol
All subjects wore a harness attached to the ceiling to pre-
vent them from falling while walking on the treadmill. The
sessions began with a rest period, in which the subjects
stood barefoot on the motor-driven treadmill (Mercury
LTmed, HP Cosmos
Ò
, Germany) [14] for the static cali-
bration of kinematic and energetic variables. Thereafter,
the subjects were asked to walk at a constant speed of
4kmh
-1
for a few minutes until a steady state was
reached and maintained for at least two minutes. Then,
energetic variables were computed for two minutes. Other
variables were simultaneously recorded for twenty seconds
and averaged for ten successive strides. The mean of each
value was used for statistical analysis. The percentage
reduction for some selected variables was calculated as
follows: the absolute difference between the mean of the
scoliosis group and the mean of the healthy subjects group,
divided by the mean of the healthy subject group. The
result was then multiplied by 100 to obtain the percentage
of change.
Statistical analysis
All the variables that followed (respect) the normal distri-
bution and equality of variance were presented in mean
(±SD). The other variables were given as medians and
quartiles [25–75%]. Statistical analysis was performed
using the software SigmaStat version 2.0, SPSS Sciences
Software GmbH, Erkrath, Germany. The significance level
was set at P B 0.05.
A one-way analysis of variance (ANOVA) or Kruskal-
Wallis One Way Analysis of Variance on Ranks (if nor-
mality and equality of variance tests not passed) was
performed to compare all gait variables between the group
of able-bodied subjects and each of the scoliosis groups. A
post-hoc test was used to identify significantly different
variables with the Bonferroni correction.
Results
In all scoliosis patient groups, the mechanical work was
significantly decreased in comparison to that of healthy
subjects (Fig. 2). On average, the external work (W
ext
)
performed by the muscles to accelerate and lift the
COM
b
and the internal work (W
int
) required to move the
limbs relative to the COM
b
were both reduced by 7 to
22% (i.e., reduced from 0.02 to 0.06 J kg
-1
m
-1
,
P \ 0.001) with the severity of the scoliosis curve.
Additionally, the totalmechanicalwork(W
tot
)was
reduced by 7 to 13% (i.e., from 0.04 to 0.07 J kg
-1
m
-1
,
P \ 0.001, Table 1). The post hoc test showed a signi-
ficant reduction as a function of the severity of the curve
for W
ext
except for scoliosis groups 1 (Cb C 20°)and2
(20 B Cb B 40°). There was no significant difference for
the W
int
between the three scoliosis groups. A significant
difference was found for W
tot
only between scoliosis
groups 1 and 3 (Cb C 40°).
Among the three spatial components of the W
ext
, the
vertical (W
ekv
)(P = 0.009) and forward (W
ekf
)(P = 0.01)
mechanical work were significantly decreased in scoliosis
patients but showed no difference between the three sco-
liosis groups (Table 1).
In all scoliosis patients, the average energy cost was
increased by 30% (i.e., from 1.8 to 2.4 J kg
-1
m
-1
,
P = \0.001) and the
_
VO
2
progressed from 9.9 to
13.8 ml kg
-1
min
-1
(P = 0.001). The muscle efficiency
was significantly decreased by 30% (i.e., from 30.2 to 20.6,
P = 0.001) when comparing all scoliosis subjects with
healthy subjects. There was no significant difference in
these energetic variables between the three scoliosis groups
(Table 1, Fig. 3).
Discussion
The present study has demonstrated an important increase
of energy cost and decrease of muscular efficiency during
1164 Eur Spine J (2009) 18:1160–1168
123
gait in AIS patients. These changes are associated with a
surprising economy of mechanical work (W
tot
). This
economy was due to the decrease of its two components,
the external work (W
ext
) performed to move the COM
b
relative to the surroundings and the internal work (W
int
)
performed to move the body segments relative to the
COM
b
.
Regarding the external work, a first explanation can be
found by examining the forward and vertical components.
The forward external work, which is necessary to accel-
erate the COM
b
in a forward direction, was progressively
reduced with the severity of the scoliosis curve from 3 to
12.5%. This is likely due to the progressive decrease of the
step length (from 0.67 to 0.64 m vs. 0.69 m in healthy
subjects). The vertical external work necessary to lift the
COM
b
was also progressively reduced from 5 to 13% and
may be explained primarily by a decrease of the vertical
displacement of the COM
b
(from 0.023 to 0.020 m vs.
0.026 m in healthy subjects). As previously reported [9,
26], the vertical displacement of the COM
b
depends on
main kinematic determinants of gait. In our study, the
restriction of pelvic and hip motion contributed to reducing
the vertical displacement of the COM
b
. In our AIS patients,
the internal work (W
int
) necessary to move the body seg-
ments relative to the COM
b
was also reduced. This
reduction may be explained by the decrease of angular
speed of the knee and ankle [21]. Effectively, the AIS
patients seem to walk carefully, as if they were carrying a
glass full of water. In sum, the decrease of W
ext
and W
int
induced a decrease of the total mechanical work (W
tot
) that
was effective even for mild scoliosis curves. It tended to be
lower in the more severe scoliosis groups, but this trend
was not significant. AIS patients seem to economize their
muscular mechanical work. This economy has never been
underlined in either experimentally restricted joint motions
or other diseases that affect locomotion [10, 11, 20, 22, 29].
In a previous study in healthy subjects, shoulder, pelvis,
and hip motion restrictions were observed when able-
bodied trunks were experimentally stiffened by bracing for
a short period of time [20]. We further observed a 15%
increase of W
ext
, which is mainly explained by a trend
toward higher vertical displacement of the COM
b
and the
loss of the pendular locomotor mechanism. When the body
is stiffened for a short period of time (less than 6 h) by an
external device that permits less motion freedom than the
joints it surrounds, it seems that the human body cannot
adapt and than produces higher mechanical work. In con-
trast, the stiffness in AIS patients is internal and perma-
nent; over the long term, it results in an adaptive
phenomenon that can explain the surprising reduction of
muscular mechanical work.
When joint restrictions are caused by an orthopedic or
neurological disease that mainly affects the lower limbs
(e.g., as in amputees or stroke patients) [10, 12], an
Table 1 Results of ANOVA on mechanical and energetic variables in 54 female subjects
Control group Scoliosis patients P value
Mean (SD) Mean (SD)
(n = 13) Cb \ 20°
(n = 12)
20 \ Cb \ 40°
(n = 13)
Cb [ 40°
(n = 16)
Mechanics
W
ext
(J kg
-1
m
-1
) 0.27 (0.02) 0.25 (0.02)* 0.25 (0.02)* 0.21 (0.02)* <0.001
W
int
(J kg
-1
m
-1
)
a
0.27 (0.25–0.27) 0.24 (0.22–0.25)* 0.24 (0.22–0.24)* 0.21 (0.19–0.24)* <0.001
W
tot
(J kg
-1
m
-1
) 0.55 (0.02) 0.51 (0.02)* 0.5 (0.03)* 0.48 (0.03)* <0.001
W
ekf
(J kg
-1
m
-1
)
a
0.32 (0.29–0.34) 0.31 (0.29–0.33) 0.30 (0.28–0.34) 0.28 (0.25–0.29)* 0.01
W
ekv
(J kg
-1
m
-1
) 0.39 (0.04) 0.37 (0.04) 0.35 (0.03)* 0.34 (0.02)* 0.009
W
ekl
(J kg
-1
m
-1
) 0.01 (0.004) 0.03 (0.1) 0.008 (0.003) 0.03 (0.07) 0.58
Recovery (%) 61.3 (4.7) 65.2 (4.3) 63.6 (5) 62.9 (4.9) 0.26
Energetics
Energy cost (J kg
-1
m
-1
) 1.8 (0.3) 2.4 (0.4)* 2.3 (0.3)* 2.4 (0.3)* <0.001
Muscle efficiency 30.2 (3.9) 23.1 (5.9)* 21.8 (3.4)* 20.6 (3.8)* 0.001
_
VO
2
(ml kg
-1
min
-1
) 9.9 (0.8) 12.8 (1.6)* 13.8 (2.8)* 13 (3.2)* 0.001
COM
b
displacement
Vertical (m)
a
0.026 (0.024–0.027) 0.023 (0.021–0.029) 0.021 (0.019–0.025) 0.020 (0.017–0.024)* 0.017
Significant differences are typed in bold and are accepted for P value B 0.05
NS Not significant, i.e. P-value [ 0.05
* Significantly different from the control group
a
Median [25–75%]
Eur Spine J (2009) 18:1160–1168 1165
123
increase of the external mechanical work due to increased
vertical displacement of the COM
b
was also observed.
Despite the surprising economic mechanical work
observed in our study, O
2
consumption was increased and
led to a significant increase in energy cost (?30%) that was
obvious in every scoliosis group as a cut-off system com-
pared to the healthy subjects (Fig. 3b). This increased O
2
consumption was not explained by the muscular mechani-
cal work requiring less O
2
consumption; instead, it can be
explained by the bilaterally prolonged activation timing of
the pelvi-femoral and lumbo-pelvic muscles [21]. The
increase of muscular timing also occurred obviously for the
mild scoliosis patients as a cut-off system. This finding
suggested the hypothesis that AIS is associated with a
significant dysfunction of the lumbo-pelvic muscles.
The prolonged timing of the EMG contraction of lumbo-
pelvic and pelvi-femoral AIS muscles was not observed
when the spino-pelvic joints were stiffened artificially by a
brace in healthy subjects in which wearing a spinal brace
experimentally for a short time did not alter muscle effi-
ciency [20]. Thus, this excessive muscular activity in AIS
patients that is even obvious in mild AIS patients is not a
direct consequence of spine stiffness.
As a result, muscular efficiency (i.e., the efficiency of
positive work production by the muscles) was reduced by
30% in comparison to that of healthy girls (Fig. 3c). This
variable may also be used as a cut-off system to differen-
tiate affected from non-affected individuals. The loss of
AIS muscular efficiency may be explained by an alteration
in the timing of the specific spino-pelvic muscles around
the scoliosis deformity. This means that muscles consume
more O
2
than just to ensure their mechanical work during
walking. This finding could raise the hypothesis that the
occurrence of very poor muscle efficiency in the lumbo-
pelvic region is balanced by an economical reaction of the
human body in order to limit the consequences of this
phenomenon.
Adolescent Idiopathic Scoliosis patients consume almost
a third more O
2
than unaffected, matched girls during the
production of this basic activity (i.e., the gait). Normal, self-
selected economical gait in our healthy subjects requires on
an average 10 ml kg
-1
min
-1
of O
2
consumption, which
corresponds to 20% of the
_
VO
2
max of an untrained normal
teen or young adult [1]. At a constant speed, the percentage
of increase of the energy cost corresponds to the percentage
of increase of
_
VO
2
: Thus, the increase of
_
VO
2
by 30% in
scoliosis patients compared to healthy subjects is compara-
ble to a gait at a speed of 6 km h
-1
in the following equation:
O
2
rate = 0.00100S
2
? 6.2 [8]. During normal walking,
scoliosis patients had to elevate their levels of physical
effort. The problem occurs when the range of O
2
con-
sumption approaches its maximum
_
VO
2
max

; at this
moment, the input of oxygen levels off and anaerobic oxi-
dation processes result in the accumulation of serum lactate
and rapid muscular intolerance to acidosis. The fact that
walking taxes less than 50% of the
_
VO
2
max in normal
subjects and does not require anaerobic activity accounts for
the perception that walking requires little effort in healthy
Fig. 3 Mechanical work, energy cost, and muscle efficiency. Each
subject (n = 54) is represented by black points. a W
tot
(J kg
-1
m
-1
)
as a function of the Cobb angle curve. b energy cost (J kg
-1
m
-1
)as
a function the Cobb angle curve. c muscle efficiency as a function of
the Cobb angle curve
1166 Eur Spine J (2009) 18:1160–1168
123
individuals [34]. However, scoliosis patients require around
35% of their
_
VO
2
max––50% more than healthy subjects––
just for walking. Therefore, it appears that scoliosis patients
exert more physical effort than healthy subjects just to walk.
For example, in amputees affected by the loss of joint motion
at different levels, the rate of energy expenditure and energy
cost increase from the ankle, to the knee, and to the hip
respectively by 3% [30], 23% [31], and 32% [34]. AIS
patients exhibit nearly the same energy cost as walking with
an immobilized hip [17]. It is thus expected that these
patients cannot bear a significant increase of effort. Barrios
et al. report that AIS patients showed earlier anaerobic
threshold and lower aerobic power, expressed by a 25%
decrease of their
_
VO
2
max [1].
This original observation suggests a new hypothesis
regarding the aetiopathogenesis of AIS. Namely, it could
be due to inefficient muscle or muscular dysfunction. This
hypothesis requires further investigation.
Therefore, it would be very interesting to follow the
same patients during their own evolution to assess the
intra-individual evolution of metabolic and mechanic
energy in order to analyze possible correlations with pro-
gression of the scoliosis curves. Additionally, it would be
very interesting to study activities requiring greater O
2
consumption, such as running and activities necessary for
the physical development of adolescents, because such
activities are more common in school physical education
programs.
Conclusions
Our hypotheses were that (1) the spinal deformations in
AIS thoraco-lumbar or lumbar main structural curve
patients will negatively impact the gait, increase the
mechanical work, and increase the energy cost of walking
and (2) the severity of the curves will correlate with the
severity of the effects in these parameters. AIS provides a
very small gait disability. In fact, the restriction of shoul-
der, pelvic, and hip motion (with the exception of a careful
gait) is so minor that it cannot be visually observed even by
an experienced clinician. With regard to the mechanics of
walking, however, our investigation paradoxically showed
a clear decrease in the muscular mechanical work associ-
ated with an increase of energy cost and a decrease in the
muscular efficiency. AIS patients exert 30% more physical
effort than healthy subjects to ensure habitual locomotion,
and this additional effort requires an important increase of
oxygen consumption. This excessive energy cost may be a
consequence of the bilateral timing activation increase of
the lumbo-pelvic and pelvi-femoral muscles. The changes
in energy parameters occur even for the mild AIS patients
like an on-off switch and could be used to differentiate
affected from non-affected individuals. These changes do
not show significant progression in relation to the severity
of the scoliosis curves.
These results suggest the hypothesis that the aetio-
pathogenesis of AIS may be due not only to a mechanical
disorder, but also to a muscular disease. More studies are
necessary to determine the causes of these excessive sco-
liosis muscle activities as well as the effects of recondi-
tioning programs and current orthopaedic or surgical
treatments.
Acknowledgment This work was supported by the Orthopedie Van
Haesendonk firm.
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    • "Data are expressed as means (standard deviation) for all variables. The sample size was based on a previous study (Mahaudens et al. 2009) that reported a net C w of 2.4 (0.4) J kg −1 m −1 and 1.8 (0.3) J kg −1 m −1 in adolescents with or without idiopathic scoliosis, respectively. To detect a 0.6 J kg −1 m −1 difference with a standard deviation of 0.4 J kg −1 m −1 , 90 % power and at the 5 % significance level, a minimum of 11 participants in both study groups was required. "
    [Show abstract] [Hide abstract] ABSTRACT: Walking in patients with chronic low back pain (cLBP) is characterized by motor control adaptations as a protective strategy against further injury or pain. The purpose of this study was to compare the preferred walking speed, the biomechanical and the energetic parameters of walking at different speeds between patients with cLBP and healthy men individually matched for age, body mass and height. Energy cost of walking was assessed with a breath-by-breath gas analyser; mechanical and spatiotemporal parameters of walking were computed using two inertial sensors equipped with a triaxial accelerometer and gyroscope and compared in 13 men with cLBP and 13 control men (CTR) during treadmill walking at standard (0.83, 1.11, 1.38, 1.67 m s(-1)) and preferred (PWS) speeds. Low back pain intensity (visual analogue scale, cLBP only) and perceived exertion (Borg scale) were assessed at each walking speed. PWS was slower in cLBP [1.17 (SD = 0.13) m s(-1)] than in CTR group [1.33 (SD = 0.11) m s(-1); P = 0.002]. No significant difference was observed between groups in mechanical work (P ≥ 0.44), spatiotemporal parameters (P ≥ 0.16) and energy cost of walking (P ≥ 0.36). At the end of the treadmill protocol, perceived exertion was significantly higher in cLBP [11.7 (SD = 2.4)] than in CTR group [9.9 (SD = 1.1); P = 0.01]. Pain intensity did not significantly increase over time (P = 0.21). These results do not support the hypothesis of a less efficient walking pattern in patients with cLBP and imply that high walking speeds are well tolerated by patients with moderately disabling cLBP.
    Full-text · Article · Jul 2015
    • "The effects of scoliosis on the efficiency and energy requirements of locomotion are relatively high [9]. Mahaudens et al. [8] calculated that the pathological gait of scoliosis entailed a 30 % increase in energy requirements when compared to the norm. Scoliosis disrupts normal biomechanics [12] as indicated by the shorter stride length, longer stride time, slower speed of gait as well as the variation in time of peak muscle activation detected in scoliotic subjects when compared to the norm. "
    [Show abstract] [Hide abstract] ABSTRACT: Several studies indicate that the gait pattern of subjects suffering from scoliosis differs from the norm. However, there is conflicting evidence regarding the source of this discrepancy. To evaluate lower limb asymmetries in selected gait variables. Study design A case–control study on lower limb asymmetries during gait which can be related to scoliosis. 31 subjects with scoliosis (Study Group - SG) and an equal comparative control sample (Control Group – CG) of subjects underwent objective gait analysis with the Vicon® motion caption system whilst walking at a comfortable speed along the gait laboratory walkway. Analysis was performed at three levels: (1) Asymmetry in the SG against asymmetry in the CG, (2) Difference in magnitude of asymmetry between the SG and CG, and (3) Global mean values in the SG vs. CG. The Paired Student T-Test was used for intra-group analysis whilst the Independent Student T-Test was used for inter-group analysis of the selected parameters, which include temporal parameters (stride length, stride time, step length, individual step speed, speed of gait, cadence, swing-to-stance ratio), ground reaction force (peak GRF values during Loading and Propulsion phases, vertical component only) and electromyography (peak EMG values and their time of onset, as a percentage of the gait cycle) of two lower limb muscles (Gastronemius and Vastus Medialis). No intra-group variation was found to be significant. However, the speed of gait was found to be significantly slower (p = 0.03) in scoliotic subjects when compared to the norm, as a result of the shorter stride length (p = 0.002 and longer stride time (p = 0.001) in the SG. Furthermore, there was statistical significance in the time of onset of EMG peaks for the Lateral Gastrocnemius (p = 0.02) with regards to inter-group difference in magnitude of lower limb asymmetry and global mean values. Scoliosis is a tri-planar deformity which has some impact on the gait pattern. This research study concludes that scoliotic subjects have a slower speed of gait due to a shorter stride length and a longer stride time, together with variations in the timing of muscle activation.
    Full-text · Article · Jul 2015
    • "Interestingly , no significant alterations in lower extremity kinematics during gait were observed at the one-year assessment for spinal deformity. Furthermore, significant improvement in muscle efficiency (i.e., total work measured by mechanical work from muscles to perform walking divided by energy cost measured by oxygen consumption during walking (Mahaudens et al., 2009)) was observed following spinal deformity fusion surgery (Tables 1 and 2). Focusing on electromyography (EMG) data during walking, a reduction in asymmetry of upper body muscle activation was discovered following spinal fusion surgery in patients with scoliosis (Hopf et al., 1998); however, no significant differences were found in either the lower extremity or the postural muscle activity duration prior to and following surgery (Tables 1 and 2). "
    [Show abstract] [Hide abstract] ABSTRACT: Objective motor performance measures, especially gait assessment, could improve evaluation of low back disorder surgeries. However, no study has compared the relative effectiveness of gait parameters for assessing motor performance in low back disorders after surgery. The purpose of the current review was to determine the sensitive gait parameters that address physical improvements in each specific spinal disorder after surgical intervention. Articles were searched with the following inclusion criteria: 1) population studied consisted of individuals with low back disorders requiring surgery; 2) low back disorder was measured objectively using gait assessment tests pre- and post-surgery. The quality of the selected studies was assessed using Delphi consensus, and meta-analysis was performed to compare pre- and post-surgical changes. Thirteen articles met inclusion criteria, which, almost exclusively, addressed two types of spinal disorders/interventions: 1) scoliosis/spinal fusion; and 2) stenosis/decompression. For patients with scoliosis, improvements in hip and shoulder motion (effect size=0.32-1.58), energy expenditure (effect size=0.59-1.18), and activity symmetry of upper-body muscles during gait were present after spinal fusion. For patients with spinal stenosis, increases in gait speed, stride length, cadence, symmetry, walking smoothness, and walking endurance (effect size=0.60-2.50), and decrease in gait variability (effect size=1.45) were observed after decompression surgery. For patients with scoliosis, gait improvements can be better assessed by measuring upper-body motion and EMG rather than the lower extremities. For patients with spinal stenosis, motor performance improvements can be captured by measuring walking spatio-temporal parameters, gait patterns, and walking endurance. Copyright © 2015 Elsevier Ltd. All rights reserved.
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