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Clinical Biomechanics 23 (2008) 769–778


www.elsevier.com/locate/clinbiomech

Effects of cadence on energy generation and absorption at


lower extremity joints during gait
Luci Fuscaldi Teixeira-Salmela a,*, Sylvie Nadeau b, Marie-Hélène Milot b,
Denis Gravel b, Luis Fernando Requião b
a
Department of Physical Therapy, Universidade Federal de Minas Gerais, Avenida Antônio Carlos, 6627, Campus Pampulha,
31270-010 Belo Horizonte, Minas Gerais, Brazil
b
École de réadaptation, Université de Montréal and Centre de recherche Interdisciplinaire en Réadaptation (CRIR),
Institut de réadaptation de Montréal, Canada

Received 31 July 2007; accepted 15 February 2008

Abstract

Background. Information regarding kinetic changes associated with walking speed is important for identifying alterations in locomo-
tor disorders caused by pathological processes, as opposed to those arising solely from altered speeds.
Methods. Fourteen healthy subjects were assessed walking at both natural and imposed cadences of 60, 80, and 120 steps/min. A 3D
motion analysis system, force platforms, and related software were used to obtain kinematic and kinetic data. Net joint powers were
calculated across cycles and the area under the positive and negative phases of the power curves provided the mechanical work generated
and absorbed at the hip, knee, and ankle. The relative contributions to the total positive and negative work across the four cadences were
calculated for each joint. ANOVAs followed by planned contrasts were used to assess the effects of laterality, joint, and cadence.
Findings. Power and mechanical work, as well as the contributions of individual joints to the total energy generated and absorbed,
were shown to be influenced by walking cadence, independent of laterality. The ankle, knee, and hip contributions to the total limb gen-
eration and absorption at the lowest cadence were 53%, 21%, and 26%, and at the highest cadence, the corresponding values were 34%,
33%, and 33%, respectively.
Interpretation. Power and mechanical work, as well as the contributions of individual joints to the total energy generated and
absorbed, were shown to be influenced by the walking cadence, independent of laterality. These findings will be helpful for identifying
walking strategies and adaptations in populations with gait disorders.
Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Gait analysis; Biomechanics; Mechanical work; Energy; Walking speed

1. Introduction tends to increase at faster walking speeds, resulting in a lar-


ger muscular force output (Den Otter et al., 2004). One of
It is well known in the study of normal human gait, that the main roles of the muscles is the control of the magni-
muscles are the main sources of energy generation and tude and duration of acceleration and deceleration of indi-
absorption. When walking, the ability to adjust the speed vidual body segments to permit safe forward progression
is an important mechanism that requires different levels (Bishop et al., 2004; Neptune et al., 2004).
of muscular activities for appropriate adaptations to Self-selected walking speed is a well-known indicator of
changes in the task demands. In general, muscle activity overall gait performance and is commonly used to assess
locomotor ability. However, gait speed alone does not con-
tribute substantially to the understanding of the nature of
*
Corresponding author. gait deficiencies nor to guide intervention protocols. By
E-mail address: lfts@ufmg.br (L.F. Teixeira-Salmela). the same token, kinematic analyses yield little information

0268-0033/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.clinbiomech.2008.02.007
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770 L.F. Teixeira-Salmela et al. / Clinical Biomechanics 23 (2008) 769–778

about the mechanisms underlying normal and abnormal (Mueller et al., 1994a, 1994b), whereas higher power gener-
movement patterns. On the other hand, kinetic analyses ation by the hip extensors in early stance was a typical, spe-
provide a better understanding of normal motor patterns cific adaptation of above (Seroussi et al., 1996) and below-
and result in new directions for diagnosing the causes of knee amputees (Gitter et al., 1991; Hermodsson et al.,
abnormal motor patterns observed in pathological gait 1994).
profiles (Olney et al., 1991, 1994). In this context, the relative contributions of each muscle
Several kinetic parameters have been proposed to evalu- group to the total energy generation or absorption should
ate gait. The moment of force parameter provides insights be studied. In normal children, Chen et al. (1997) investi-
about the predominant muscle groups at a given joint and gated the influences of walking speed on mechanical joint
about the level of the mechanical effort that is produced power during gait and demonstrated that the relative con-
when relatively expressed to the maximal force capabilities tributions to mechanical work of muscles about the knee
(Milot et al., 2006; Requião et al., 2005). The assessment of and hip were positively correlated with speed, while nega-
the joint power parameter is more sensitive to instanta- tively correlated with ankle muscles. Nadeau et al. (2001)
neous muscle effects to generate or absorb energy, but does investigated the relative contributions to energy generation
not take into account the duration of force application. for stroke and healthy subjects walking at similar speeds
Work parameters, on the other hand, integrate the power and observed that for the former, they were greater when
curve over time and provide, in some cases, additional originated from the hip flexors, whereas for the later, the
meaningful measures (Winter, 1991) to understand normal plantarflexors predominated. Thus, the estimation of the
(Chen et al., 1997; Siegel et al., 2004; Winter, 1983a) and relative contribution of each joint to the total energy gen-
abnormal walking patterns (Mansour et al., 1982; McGib- erated and absorbed during gait at different speeds seems
bon et al., 2001; Olney et al., 1991, 1994; Teixeira-Salmela to be a useful approach to understand the nature, extent,
et al., 2001). Positive work performed during concentric and degree of compensation across joints and to suggest
contractions, results in energy flow from muscles to the seg- more efficient methods of correction. Moreover, informa-
ments to accelerate the body, whereas negative work, orig- tion which is related to kinetic changes to walking speed
inating from eccentric contractions, produces energy flow is important for identifying alterations in locomotor disor-
from the segments to the muscles to decelerate the body. ders caused by pathological processes, as opposed to those
The interplay between these energy sources facilitates suc- arising solely from altered speeds.
cessful progression during walking (Chen et al., 1997; Win- Therefore, the purpose of the present study was to
ter, 1983). employ an analytical model to estimate the effects of walk-
When walking on level surfaces, the ankle plantarflex- ing cadence and laterality on the positive and negative
ors, hip flexors, and hip extensors are the main muscle mechanical work performed by the hip, knee, and ankle
groups that contribute to energy generation in the sagittal muscles in the sagittal plane. According to Winter
plane (Chen et al., 1997; Olney et al., 1994; Winter, 1983, (1983b), cadence does not affect the energy generation
1991). Previous studies have shown high correlations and absorption pattern shapes over a stride and it is largely
between positive power bursts of these muscle groups and controlled by the mechanical power generation and
gait velocity or cadence both with normal (Sadeghi et al., absorption. Therefore, it was decided to use cadence as
2001), low-performing elderly (Graf et al., 2005), and path- the controlling parameter in the present study.
ological subjects (Mueller et al., 1994a, 1994b; Olney and
Richards, 1996; Teixeira-Salmela et al., 2001). The knee 2. Methods
joint muscles act mainly eccentrically and the rate of
absorption of energy is greater with increases in walking 2.1. Participants
speed (Olney et al., 1994; Teixeira-Salmela et al., 2001;
Winter, 1983), while negative work at the hip and ankle Fourteen healthy volunteers participated in the study,
also results in increases at higher walking speeds. recruited from the community, who had no previous his-
Because decreasing gait speed or cadence is commonly tory of lower limb injuries and showed no obvious gait
observed in locomotor disorders, information on kinetic abnormalities. All participants provided consent prior to
changes with gait speed or cadence in normal subjects is their evaluation, based on ethical approval from the local
important to pinpoint specific modifications related to the research review board. Data related to the mechanical level
pathology. The study of variations in positive and negative of effort during gait at different cadences have been pub-
energy contributions would provide baseline data and yield lished in a previous study for this group of participants
information that would be useful in understanding and (Requião et al., 2005) and used as comparative data in
treating gait deviations. Moreover, the interaction between another study (Milot et al., 2006).
different muscle groups in generating and absorbing power
is relevant for the understanding the compensatory mecha- 2.2. Gait assessment
nisms in pathological conditions. For example, patients
with diabetic peripheral neuropathy were able to attenuate Participants walked with their own low-heeled shoes
the decreased push-off by emphasizing hip flexor muscles along a nine-m walkway over three embedded force plat-
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L.F. Teixeira-Salmela et al. / Clinical Biomechanics 23 (2008) 769–778 771

forms of standardized dimensions. First, subjects were approach (Winter, 1991) performed with Kingait3 software
required to walk at their natural cadence, followed by three (Mishac Kinetics, Waterloo, Canada) was used to estimate
other imposed cadences of 60, 80 and 120 steps/min, con- the net moments at the ankle, knee and hip joints.
trolled by a metronome. Five walking trials for each side Net joint powers (P) were calculated for each instant in
were collected at the four cadences, for a total of 40 trials. time as the product of net moments across the joint (M)
A successful trial was defined as one in which the subject and the relative angular velocity between the adjacent limb
appropriately contacted the force platform, i.e., the subject segments (x). When the product (M * x) was positive, the
hit one force platform with one foot, keeping the metro- muscles generated energy by contracting concentrically and
nomic rhythm. when the product was negative, the muscles absorbed
A three-dimensional (3D) Optotrak motion analysis sys- energy by contracting eccentrically. The power curves at
tem, three AMTI (Advanced Medical Technologies, New- the hip, knee, and ankle were analyzed on the basis of all
ton, MA, USA) force platforms, and related software cadences and all phases of power generation and absorp-
were used to obtain kinematic and kinetic data. The accu- tion were identified. The area under the positive phase of
racy for the Optotrak system and for the location of the the power curve provided the mechanical work generated
center of pressure of force platforms was 1 mm and 3 mm (Wpositive; Eq. (1)) at the hip, knee, and ankle, whereas
(RMS mean values), respectively. the integral of the negative phase (Wnegative; Eq. (2)), pro-
Prior to data collection, infrared markers were placed vided the absorbed work (Winter, 1983)
bilaterally on the following locations: foot (lateral heel, Z tf
dorsum, fifth metatarsal head), leg (lateral malleolus, mid W positive ¼ P dt for P > 0 ð1Þ
J
shank, and head of fibula), thigh (greater trochanter, ti
Z tf
mid-thigh, and lateral femoral condyle), pelvis (left and
right posterior superior iliac spine, left iliac crest), trunk W negative
J ¼ P dt for P < 0 ð2Þ
ti
(L3, T12 spinous process, right and left at the T8 level, C7
spinous process, and right and left acromium), and head
where J refers to the joint (ankle, knee or hip), P to the
(right and left occipital). In addition, 13 specific anatomical
joint power, and ti and tf to the initial and final gait cycle
points on the feet (heel posterior point, tip of foot), shanks
times, respectively. For all cadences, the energy generated
(medial malleoli), thighs (medial femoral condyles), pelvis
and absorbed at the ankle, knee, and hip was computed
(right and left ASIS, and iliac crests) and trunk (left gleno-
without consideration to the muscle groups involved at a
humeral joint) were digitized with a probe to define the
given joint.
local axis of each segment. Anthropometric measurements,
In addition, for each cadence, the work generated by the
consisting of length and diameter of segments, using the
flexors and extensors for all joints were summed to produce
landmark locations as references, were manually collected,
the total positive work (Eq. (3)) of each lower limb
along with body mass and height. Stride characteristics
ðW positive
Limb Þ. The same was carried out for the total absorbed
were recorded with three foot-switches located on the soles
work (W negative
Limb ; Eq. (4))
of their shoes (heel, mid-foot, and tip of the foot).
W positive
Limb ¼ W positive positive positive
Ankle þ W Knee þ W Hip ð3Þ
2.3. Data processing negative negative negative negative
W Limb ¼ W Ankle þ W Knee þ W Hip ð4Þ
The coordinate data, sampled at 60 Hz, were digitally
filtered using a 4th-order Butterworth zero-lag filter, with The relative contributions (Cont) of each joint to the
a cut-off frequency of 6 Hz. The data analysis (Mishac total positive or total negative work was calculated by
Kinetics, Waterloo, Canada) was used to calculate the rel- dividing the work values generated or absorbed by each
ative angles from a rotation matrix using a cardanic joint by the total energy value, and multiplied by 100.
sequence, so that the local x, y and z axes corresponded, For example, the contribution to the positive work by the
respectively, to abduction–adduction, longitudinal rotation ankle (Eq. (5)) in a gait cycle was calculated as followed:
and flexion–extension for the hip and knee joints, and ever- .
sion–inversion, transverse rotation, and dorsiflexion–plan- Contpositive
Ankle ¼ W positive
Ankle W positive
Limb
tarflexion for the ankle joint. .
Ground reaction forces were collected at 600 Hz with ContAnkle ¼ W Ankle W negative
negative negative
Limb ð5Þ
three force platforms embedded in the nine-m walkway.
These data were also filtered with a 4th-order Butterworth Finally, the joint contributions to the total work
zero-lag filter, with a cut-off frequency of 10 Hz and resam- observed in a gait cycle were also computed, using Eq.
pled at 60 Hz to match the kinematic data. The foot con- (6) as an example for the ankle
tact and ground reaction forces served to determine the h i.h i
gait cycles, which were normalized to 100%. For each ContAnkle ¼ W positive þ W negative
W positive
þ W negative
Ankle Ankle Limb Limb
imposed cadence, the three trials showing the closest
cadences were averaged for each side. An inverse dynamic ð6Þ
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2.4. Data analyses 3.2. Power profiles

All statistical analyses were carried out using SPSS for The overall average patterns for the ankle, knee, and hip
Windows. Descriptive statistics and tests for normality for the dominant side across all cadences are presented in
(Shapiro-Wilk) were performed for all outcome variables. super-imposed graphs. The curve patterns had several
Differences in spatio-temporal parameters between the four characteristics that were common to all subjects. At the
cadences were identified by repeated measures ANOVA hip, three major power phases were observed (Fig. 1A):
followed by planned contrasts with a significance level of
a < 0.05.
Since no main effects for laterality were found (see Sec- A 200
60
tion 3), the data for the dominant and non-dominant sides
150 80
were collapsed and a two-way within-factor repeated mea-
Natural
sures ANOVA was used to assess joint and cadence effects H3
100 120
and interactions. Whenever a main effect or interaction
effect was significant, focused contrasts were performed

Watts
50
H1
to locate the differences. Bonferroni corrections for multi-
ple comparisons in terms of cadence conditions were
0
applied to contrast results, changing the significance level
from 0.05 to 0.008 (0.05/6). Gait power profiles were
-50
described, but not statistically analyzed, to demonstrate
H2
changes associated with the cadence.
-100
0 10 20 30 40 50 60 70 80 90 100
Percent of Gait Cycle
3. Results
B 200
60
Fourteen healthy subjects (seven women and seven men)
80
completed the evaluation. The mean age, stature and body 150
Natural
mass were 46.0 (±13.3) years, 1.70 (±0.10) m, and 72.0
120
(±14.9) kg, respectively. Only one subject was left-side 100
dominant.
Watts

50
K2

3.1. Spatio-temporal measures


0

Table 1 presents the description of the spatio-temporal -50


variables for the natural and imposed cadences and the
actual cadences were close to the prescribed ones. Gait K1 K3 K4
-100
speed and stride length increased with cadences and greater 0 10 20 30 40 50 60 70 80 90 100
variability was observed for the natural and 120 prescribed Percent of Gait Cycle
cadences. ANOVA revealed that the four cadences pro-
duced highly significant gait speed differences C A2
200
(P = 0.0001). However, no differences were found between
the natural and the imposed 120 cadences (P = 0.16). 60
150 80
Natural
100 120
Watts

Table 1
50
Means (±SD) and range [min–max] of spatio-temporal measures for the
dominant side across cadences (n = 14)
0
Measure Cadence
60 80 Natural 120
-50
Cadence 65.8 ± 4.8 83.7 ± 2.1 105.3 ± 13.7 115.1 ± 12.0
reached [61.0–75.7] [79.3–85.7] [77.2–129.8] [95.9–141.5] A1
-100
(steps/min)
0 10 20 30 40 50 60 70 80 90 100
Stride length 1.2 ± 0.1 1.3 ± 0.1 1.4 ± 0.2 1.5 ± 0.2
(m) [1.0–1.4] [1.1–1.5] [1.2–1.7] [1.1–1.7] Percent of Gait Cycle
Speed (m/s) 0.67 ± 0.09 0.92 ± 0.10 1.25 ± 0.24 1.42 ± 0.22
Fig. 1. Power profiles (Watts) across cadences: (A) at the hip, (B) at the
[0.51–0.82] [0.75–1.07] [0.79–1.53] [1.08–1.85]
knee, and (C) at the ankle joint.
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the power was positive during the first half of the stance the ANOVA revealed significant interactions between
phase, negative during the second half, and became posi- joints and cadences, subsequent analyses used planned con-
tive during late stance (pull-off phase). For the knee, four trasts for comparisons of joint or cadence effects.
major power phases were identified, with power being pri- For the contributions to energy generation (Table 2 and
marily negative (Fig. 1B). As shown in Fig. 1C, two major Fig. 2B), analyses showed significant decreases at the ankle
phases were observed at the ankle: negative power was joint and significant increases for the hip joint across all
recorded at early and mid-stance with a large positive peak cadences (P < 0.001), except for those at the hip between
at late stance. As shown in Fig. 1A–C, a common pattern natural and the 120 cadence. For the knee, no differences
for all joints was reflected by a consistent trend towards were found between 60 and 80 (P = 0.41), and between nat-
higher values of power bursts for all joints as the cadence ural and the 120 cadence (P = 0.21). Moreover, there was a
increased. joint effect for all cadences (P = 0.001).
For the contributions to energy absorption (Table 2 and
3.3. Energy variables Fig. 3B), planned contrast analyses showed significant dif-
ferences for the knee across all cadences (P = 0.001), except
3.3.1. Joint and cadence effects for the natural and the 120 cadence, which were not signif-
Table 2 provides the descriptive data related to energy icantly different (P = 0.09). No differences were found at
generated and absorbed, as well as the energy contributions the hip joint and for the ankle between 60 and 80
at each joint for the natural and imposed cadences for all (P = 0.08), and between natural and the 120 cadence
subjects. Figs. 2 and 3 illustrate the mechanical energy gen- (P = 0.51). Moreover, there was a joint effect for all
erated and absorbed, as well as the relative contributions of cadences, except for the knee and hip at the lower cadences
the hip, knee, and ankle joints across cadences. of 60 and 80 and for the ankle and hip for higher cadences
For respective energy generation and absorption, signif- (natural and 120). The results indicated that at lower
icant effects for joint (F = 143.54; df = 2; P < 0.001 and cadences (60 and 80), similar contributions were observed
F = 3.98; df = 2; P = 0.03), cadence (F = 36.64; df=2; for the knee and hip, whereas at higher cadences (natural
P < 0.001 and F = 22.98; df = 2; P < 0.001), and joint-by- and 120), the ankle and hip showed similar contributions.
cadence interactions (F = 10.79; df = 6; P < 0.001 and
F = 12.95; df = 6; P < 0.001) were demonstrated. Since 4. Discussion
ANOVA revealed significant interactions between joints
and cadences, subsequent analyses used planned contrasts The present study assessed the work generation and
for comparisons for joint or cadence effects. absorption, as well as the relative contributions of each
For the energy generating values (Table 2 and Fig. 2A), lower extremity joint to the total positive and negative
planned contrast analyses showed significant differences for work during gait, in relation to cadence. Mechanical work
all joints across all cadences (P < 0.001), except between about the lower extremity joints was shown to be influ-
the natural and 120 cadence. Moreover, there was a joint enced by the walking cadence, independent of the side of
effect for all cadences (P < 0.001), except between the ankle the body. In addition, the contributions of the individual
and hip at the imposed cadence of 120. joints to the total generated and absorbed energy during
For the energy absorbing values (Table 2 and Fig. 3A), gait was also influenced by cadence, suggesting that speed
significant differences were found only for the knee and hip differences should be minimized when comparing power
joints (P < 0.001) across all cadences, except between the values between walking trials in other studies. Four main
natural and 120 cadence. Statistical analyses revealed that issues will be discussed in the following sections.
ankle energy was significantly higher than at the knee
and hip energy at lower cadences (60 and 80), while the 4.1. Spatio-temporal measures
knee energy level was significantly higher than the hip
and ankle energy for higher cadences (natural and 120 The four investigated cadences resulted in mean speeds
cadence). ranging from 0.67 to 1.42 m/s, which were very similar than
those of 0.65–1.35 m/s assessed with healthy older adult
3.3.2. Joint contributions subjects (Teixeira, 1998). In the present study, these
ANOVA revealed that the contributions to energy gen- cadences were chosen to match those usually demonstrated
eration and absorption at the individual joints also chan- by subjects with locomotor disabilities walking at natural
ged with cadence (Table 2). Analyses for relative speeds, whose speed values rarely surpass 1.42 m/s (Olney
contributions to energy generation demonstrated signifi- et al., 1991, 1994; Olney and Richards, 1996; Teixeira-Sal-
cant effects for joint (F = 143.54; df = 2; P < 0.001 and mela et al., 2001). No differences in gait speed were found
F = 3.98; df = 2; P = 0.03) and joint-by-cadence interac- between the higher natural cadences and the imposed one
tion (F = 10.79; df = 6; P < 0.001 and F = 12.95; df = 6; of 120 steps/min. The reasons behind these non-significant
P < 0.001), respectively. No main effects were observed differences may be related to the large variations across
for the relative contributions to energy absorption; how- subjects. It appears that some subjects had a higher natural
ever, analyses showed joint-by-cadence interactions. Since cadence than the 120 steps/min, while others found it diffi-
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Table 2
Means (±SD), range [min–max] of positive and negative work (Joules) and contributions (%) to positive and negative work at ankle, knee, and hip joints across cadences (n = 28)

L.F. Teixeira-Salmela et al. / Clinical Biomechanics 23 (2008) 769–778


Ankle Knee Hip Limb(ankle+knee+hip)
P þ P P þ P þ
W+ W ðW þ W  Þ W+ W ðW þ þ W  Þ W+ W ðW þ W  Þ W+ W ðW þ W  Þ
60 steps
Mean 13.4 14.6 28 3.6 7.6 11.2 5.5 8.5 14 22.5 30.7 53.2
SD 3.7 4.5 9.7 2 2.6 5.3 2.5 5.4 6.8 8.5 11.14 18.5
Range [6.5–19.2] [10–28.3] [18–42] [0.8–8.0] [1.9–12.1] [3–20] [2.3–11.6] [0.7–23.4] [5–30] [10–33] [13–45] [29–75]
Cont (%) to WLimb 59.8 47.6 52.7 15.8 24.9 21 24.4 27.6 26.3 100 100 100
80 steps
Mean 15 14.3 29.3 4.3 11.3 15.6 8.3 10 18.3 27.6 35.6 63.2
SD 4.5 4.3 10.6 2.4 3.8 7.2 4.5 4.8 7.7 11 12.5 22.2
Range [8.3–23.6] [9.4–23.4] [18–46] [0.3–9.2] [4.8–20.9] [5–27] [3.7–24.5] [4.7–24.6] [9–33] [12–55] [19–55] [36–93]
Cont (%) to WLimb 54.4 40.3 46.5 15.6 31.7 24.6 30 28 28.9 100 100 100
Natural
Mean 19.2 12. 5 31.7 7 18.6 25.6 13.7 13 26.7 39.9 44.1 84
SD 5 4.5 7.7 3.1 6.7 10.4 7 5.8 10.3 13.2 13.9 25
Range [9.3–29.5] [6.9–22.9] [20–47] [2.9–13.7] [10–38.1] [15–52] [4–28] [5.5–26.0] [13–52] [23–67] [24–81] [57–139]
Cont (%) to WLimb 48.1 28.3 37.7 17.6 42.2 30.5 34.3 29.5 31.8 100 100 100
120 steps
Mean 19.7 12.3 32 8.5 22.3 30.8 17.1 14.5 31.6 45.3 49.1 94.4
SD 5.5 4.7 10.22 3.5 7.2 12.5 8.8 6.8 14.2 17.8 16.8 33.1
Range [11–33.7] [5–23.4] [21–48] [2.7–16.2] [7.5–35.9] [10–52] [5.5–47.8] [4.1–28.9] [12–77] [19–90] [17–77] [45–175]
Cont (%) to WLimb 43.5 25.1 33.9 18.7 45.4 32.6 37.8 29.7 33.5 100 100 100
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30
A A 30
Ankle

Mechanical Energy (J)


25 Ankle
Mechanical Energy (J)

25 Knee
Knee
Hip
Hip
20 20

15
15

10
10
5
5
0
0 60 steps 80 steps Natural 120 steps
60 steps 80 steps Natural 120 steps
B 70 Ankle
80
B 60 Knee
70 Hip
Ankle 50
60 Knee
Hip 40

%
50
30
(%)

40
20
30
10
20
0
10 60 steps 80 steps Natural 120 steps

0 Fig. 3. (A) Mechanical energy absorption at the hip, knee, and ankle
60 steps 80 steps Natural 120 steps joints (Joules; J) across cadences. (B) Relative contributions of the hip,
knee, and ankle joints (percentages; %) to energy absorption across
Fig. 2. (A) Mechanical energy generation at the hip, knee, and ankle
cadences.
joints (Joules; J) across cadences. (B) Relative contributions of the hip,
knee, and ankle joints (percentages; %) to energy generation across
cadences.
different strategies to accomplish the task. It is possible that
some subjects may have used their plantarflexors more
cult to reach the prescribed 120 steps/min cadence. The net than hip flexors or extensors, while others may have done
result was an overlap of the distributions of gait speed mea- the reverse. In fact, Vardaxis et al. (1998) suggested that
sured at the natural and 120 cadence resulting in non-sig- the variability observed in able-bodied gait may be the
nificant differences. Considering that energy changes were result of multiple normal dynamic strategies employed by
closely associated with differences in gait speed, it was different subjects and should be considered in studies inves-
not surprising that differences between the natural and tigating gait.
imposed 120 cadence for energy parameters did not reach Cadence influenced the mechanical work performed by
statistical significance. the muscles acting at the hip, knee, and ankle. This sup-
ported previous findings (Chen et al., 1997) that the total
4.2. Cadence effects energy generated and absorbed by the knee showed the
largest increases (175%) in response to cadence changes.
The influences of speed on kinetic parameters has been The hip also showed substantial increases of 126%, whereas
extensively investigated (Bishop et al., 2004; Chen et al., the ankle demonstrated the smallest changes. The present
1997; Den Otter et al., 2004; Graf et al., 2005; Miyoshi findings supported the evidence of a trade-off between the
et al., 2004; Olney et al., 1994) and independent of the hip and ankle joints, which were also shown by Graf
selected population, methodology, and parameters used, et al. (2005) and could reflect adjustments of the lower limb
the effects of cadence were consistent. Kim and Eng to more efficiently meet different task demands or to atten-
(2004) observed that the magnitude of kinematic and uate fatigue and share the effort across muscles when the
kinetic gait profiles were significantly related to gait speed cadence increases. Previous analyses of the level of effort
in all three planes. Significant correlations between the during the period of energy generation for this group of
same work phases across cadences indicate the same pat- subjects has revealed that the level of effort increased with
tern with increases in cadence. However, the absence of sig- gait cadence but the increases were more pronounced for
nificant correlations between different work phases at a the hip muscles (Requião et al., 2005). Energy generation
given cadence indicates that the subjects did not adopt con- around the knee was minimal compared to that generated
sistent patterns to generate or absorb work, i.e., they used at the ankle and hip joints, reinforcing the findings that
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776 L.F. Teixeira-Salmela et al. / Clinical Biomechanics 23 (2008) 769–778

the knee muscles mainly absorb, rather than generate instructed to walk at various speeds, which were selected
energy (Olney et al., 1991; Winter, 1983). post-hoc and subsequently classified into three categories
Negative work supplied by the knee has been reported based on their actual walking speeds.
to be highly correlated with speed and one of the best pre- Regarding the respective contributions to energy
dictors in gains in walking performance (Olney et al., 1994; absorption, increases were seen at the hip and knee joints,
Winter, 1983). It appears that at increased cadences, mus- but the most striking changes were observed at the knee,
cles generate and absorb energy at faster rates. Important which increased from 25% at the lowest cadence to 45%
increases observed at the knee joint might be the result of at the highest. Energy absorption is not only associated
the work of numerous biarticular muscles in promoting with an active contraction but passive contributions to
energy flow between segments and transferring energy from energy absorption should also be considered. Neptune
the leg to the thigh to increase overall gait speed. The tran- et al. (2004) observed that forces developed from stretched
sition patterns between the energy generation/absorption passive hip structures assisted plantarflexors during the
of the hip, knee, and ankle muscles suggest a shift of work swing initiation. By the same token, the passive energy
to larger muscle groups at faster cadences. This shift of absorbed by the rectus femoris at the end of stance may
energy to larger and more proximal muscle groups may have assisted hip flexors in limb propulsion.
permit muscles to work at a lower percentage of their max- It is interesting to note how the total contributions at
imum capacity and, therefore, optimize energy consump- each joint to the sum of the total limb generation and
tion during gait. absorption changed when cadences were increased. At the
For the different behaviors of the muscles at the ankle, lowest cadence, the ankle, knee, and hip contributed
which showed the smallest increases in work values in 53%, 21%, and 26%, respectively, however, at the fastest
response to changes in cadence, there are parallel findings cadence, these discrepancies were less evident and the con-
in the literature. Andriacchi et al. (1977) demonstrated that tributions by each joint to the total energy were more bal-
the muscle moment about the hip and knee showed greater anced. For instance, at the highest cadence, 34% of the
dependencies on speed, whereas, the moment at the ankle total energy was provided by the structures about the
did not substantially change. In addition, studies with chil- ankle, 33% from the knee and 33% from the hip, indicating
dren (Chen et al., 1997), adults (Winter, 1983), and with that all three joints played similar roles in contributing to
low-performing elderly subjects (Graf et al., 2005) have the sum of the total energy used. These findings suggest
shown that the work at the ankle demonstrated the least that, at faster cadences, the power-energy capability of
sensitivity to speed variations. the knee muscles was functionally relevant, since they were
responsible for about one third of the total work performed
4.3. Contributions to energy generation and absorption at the highest cadence. Therefore, the contributions of the
knee as a energy modulator should not be underestimated.
When expressed as a percentage of work contributions, Although the positive and negative work increased at
the variations of behavior of the ankle, knee, and hip in about the same amount for the knee and hip joints across
relation to cadence, become even more obvious. The con- cadences, they were actually quite different. There were rel-
tributions to work from the muscles about the knee and atively small increases in the positive work for the knee
hip showed increases at higher cadences, while those from (136%) and much greater changes at the hip (221%). On
the muscles about the ankle substantially decreased. For the other hand, there were much larger increases in the neg-
instance, at the lowest cadence, about 60% of the total ative work for the knee (192%) and less for the hip (70.6%).
energy generated resulted from the muscles about the It is also important to note that the ankle had a larger
ankle. However, when the cadence was up to 120 steps/ absolute increase in positive work (6.3 J) across cadences
min, only 44% of the total energy generated originated than did the knee (4.9 J), a value that was about half of
from these muscles. The contributions of the muscles about the amount of the positive work at the hip (11.6). However,
the hip to the total energy generated increased from 24% at the negative work at the ankle actually decreased (2.3 J,
the lower to 38% at higher cadences, whereas knee contri- 16%) across cadences, whereas increases of 6.0 and 14.6 J
butions increased from 16% to 19%, indicating large contri- were found for the hip and knee, respectively.
butions of hip muscles for speed modulation. In the present study, only power and work performed
Few studies have evaluated the relative contributions of in the sagittal plane during concentric and eccentric
the muscles about the ankle to the total energy generated contractions were evaluated and it was observed that the
during gait at different speeds, but differences in the assess- differences between the positive and negative values for
ment protocols make comparisons difficult. The findings of the total limb work, were always higher for the negative
the present study are somewhat in agreement with those of work, which supported the limitations of the sagittal plane
Chen et al. (1997) on contributions of the lower extremity model. It has been reported that with normal subjects,
joints to the total work generated within three walking contributions to kinetic energy existed from sagittal and
groups of healthy children. In the present study, cadences non-sagittal plane motions (Vardaxis et al., 1998). In fact,
were tightly controlled, while in the study of Chen et al. Graf et al. (2005) reported that the larger transverse pelvic
(1997), they were not strictly imposed. Participants were rotations employed by low-performing subjects may be a
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compensatory mechanism to increase step length and gait Den Otter, A.R., Geurts, A.C., Mulder, T., Duysens, J., 2004. Speed
speed. In addition, body support and forward progression related changes in muscle activity from normal to very slow walking
speeds. Gait Posture 19, 270–278.
were found to occur because power redistribution between Eng, J.J., Winter, D.A., 1995. Kinetic analysis of the lower limbs during
the legs and trunk occurred through muscular force gener- walking: what information can be gained from a three-dimensional
ation, regardless of whether produced from concentric, model? J. Biomech. 28, 753–758.
isometric, or eccentric activity. It could be argued that Gitter, A., Czerniecki, J.M., DeGroot, D.M., 1991. Biomechanical
underestimation of power and work might have occurred analysis of the influence of prosthetic feet on below-knee amputee
walking. Am. J. Phys. Med. Rehabil. 70, 142–148.
because of the absence of motion evaluation in the frontal Graf, A., Judge, J.O., Õunpuu, S., Thelen, D.G., 2005. The effect of
and transverse planes and that produced by isometric walking speed on lower-extremity joint powers among elderly adults
muscle activity, especially for the hip joint. For instance, who exhibit low physical performance. Arch. Phys. Med. Rehabil. 86,
if the lower limb was laterally rotated, so that the adduc- 2177–2183.
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male trans-tibial amputees: a comparative study with healthy subjects
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However, the major portion of this movement is Kim, C.M., Eng, J.J., 2004. Magnitude and pattern of 3D kinematic and
performed in the sagittal plane, because the goal of kinetic gait profiles in persons with stroke: relationship to walking
locomotion is to support body weight against gravity speed. Gait Posture 20, 140–146.
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and eccentric works are performed (Nadeau et al., 2003). Biomech. 34, 481–490.
Milot, M.H., Nadeau, S., Gravel, D., Requiao, L.F., 2006. Bilateral level
of effort of the plantar flexors, hip flexors, and extensors during gait in
5. Conclusions hemiparetic and healthy individuals. Stroke 37, 2070–2075.
Miyoshi, T., Shirota, T., Yamamoto, S., Nakazawa, K., Akai, M., 2004.
The findings demonstrated that the performance of the Effect of the walking speed to the lower limb joint angular displace-
dominant and non-dominant sides was very similar, inde- ments, joint moments and ground reaction forces during walking in
pendent of the joint or cadence. Power and mechanical water. Disabil. Rehabil. 26, 724–732.
Mueller, M.J., Minor, S.D., Sahrmann, S.A., Schaaf, J.A., Strube, M.J.,
work, as well as the contributions of individual joints to 1994a. Differences in the gait characteristics of patients with diabetes
the total energy generated and absorbed, were shown to and peripheral neuropathy compared with age-matched controls. Phys.
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ality. The ankle, knee, and hip contributions to the total Mueller, M.J., Sinacore, D.R., Hoogstrate, S., Daly, L., 1994b. Hip and
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The present findings provide baseline data for identifying and compensatory strategies in gait. Crit. Rev. Phys. Rehabil Med. 13,
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analysis of the stair climbing task in healthy adults over 40 years: what
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Olney, S.J., Griffin, M.P., Monga, T.N., McBride, I.D., 1991. Work and
Canadian Institute of Health Research, CAPES (Brazil- power in gait of stroke patients. Arch. Phys. Med. Rehabil. 72, 309–
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Santé du Québec (FRSQ). Olney, S.J., Griffin, M.P., McBride, I.D., 1994. Temporal, kinematic, and
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