ELSEVIER Human Movement Science 16 (1997) 243-258

Functional gait asymmetry in

Heydar Sadeghi a,b~c, * , Paul Allard

able-bodied subjects

a,b, Morris Duhaime b,d

a Department of Physical Education, University of Montreal, Montreal, PQ, Canada b Research Center, Saint-Justine Hospital, 3175 Cote Ste-Catherine, Montreal, PQ, H3T ICS, Cana&

’ Department of Physical Education, University of Tarbiat Moallem, Tehran, Iran ’ Orthopaedic Surgery, Shriner’s Hospital, Montreal, PQ, Canada

Abstract

Symmetry is assumed in unilateral gait studies or when pooling right and left limb data. The purpose of this study was to identify which muscle powers and associated mechanical energies were related to the support and propulsion functions using Principal Component Analysis (PCA). Nineteen able-bodied male subjects participated in this study. They were all right-hand and leg dominant. Simultaneous bilateral three-dimensional data were collected from an eight-camera

video system and two force plates. The PCA method was used to reduce and categorize the peak muscle powers and mechanical energies calculated at the hip, knee and ankle in each plane. Student’s t-test for paired data was applied to determine significant differences between the identified gait parameters. The limb which had a propulsion function was characterized by a

strong third hip power at push off. Most of the parameters identified by the PCA were associated with the hip, and were mainly in the sagittal plane. These parameters were concentrated during push-off. There was a secondary support function which occurred during midstance. For the limb having a supporting function, most of its activities were associated with the knee, and were spread throughout the stance phase.

PsycINFO classification: 2330

Keywords: Gait analysis: Symmetry; Principal component analysis

* Corresponding author. E-mail: sadeghih@ere.umontreal.ca, Tel.: + 1 514 345-4740, Fax: + I 514

345-4801.

0167-9457/97/$17X@ Copyright 0 1997 Elsevier Science B.V. All rights reserved.

PII SO1 67-9457(96)00054- I

244 H. Sadeghi et al./Human Moc;ement Science I6 (1997) 243-2.58

1. Introduction

Many gait analyses have focused on the biomechanical aspects of the right limb, assuming similarity with the contralateral limb. Using bilateral three-di- mensional electrogoniometers in twelve able-bodied subjects, Hannah et al. (1984) have shown joint motion symmetry between the hips in all three planes and at the knees in the sagittal plane during natural walking. Hamill et al. (1984) found no significant difference between the limbs in 11 vertical, 5 anterior-post- erior and 4 medio-lateral characteristics of ground reaction forces in walking and running. These results were later confirmed by Menard et al. (19921, in a study where eight normal subjects walked at their natural speed.

However, there are a number of bilateral investigations where gait asymmetry was documented. Rosenrot et al. (1980) reported that the duration of the initial and terminal double support periods were not identical, as would be expected in young healthy subjects. Crowe et al. (1993) reported a consistent asymmetry in the oscillation of the body center of mass using ground reaction force data. According to Wheelwright et al. (1993), gait asymmetry may be related to the position of the foot during the swing phase, reflecting the subject’s laterality. Though Gunderson et al. (1989) concluded that asymmetry cannot be predicted by lateral dominance, Ounpuu and Winter (1989) found some evidence to suggest that the plantar-flexor electromyographic (EMG) activity is related to limb dominance. Arsenault et al. (1986) also found asymmetries in EMG profiles.

The aim of locomotion is to support the body against gravity while generating movements to propel the body forward. It requires precise coordination between the tasks of propulsion, and balance (Winter, 1990). In recent gait studies, asymmetry has been explained by a functional behaviour of lower extremities. Hirasawa (1981) claimed that the left and right lower limbs have a supporting and a moving function, respectively. For 53 males and 39 females walking at slow, free and fast walking speeds, Hirokawa (1989) associated propulsion with the right limb while the left limb was found to be responsible for support. Allard et al. (1996) were among the first to report simultaneous bilateral three-dimen- sional inverse dynamic gait data in 19 able men. Asymmetries in the peak muscle powers as well as in their corresponding energies were found. Though both limbs generated the same total energy, the higher total energy absorption in the right limb was attributed to its control.

The functions of propulsion and control of the lower limbs have been clearly identified during gait, but the biomechanical parameters associated with each of them are still to be identified. Though temporal and phasic gait parameters, joint

H. Sadeghi et al./Humm Movement Science 16 (1997) 243-258 245

angles and muscle moments may be used to characterize gait patterns, muscle powers are more convenient since they lump both kinematic and kinetic information. To our knowledge, there have been only a few studies that dealt with symmetry in simultaneous bilateral three-dimensional gait analyses.

The purposes of this study were (a) to identify the three-dimensional peak mechanical muscle powers and the mechanical energies developed by the lower extremities during able-bodied gait using Principal Component Analysis, and (b) to determine which of these gait parameters were related to propulsion and support.

2. Methods

Nineteen healthy young adult men recruited from the Department of Physical Education at the University of Montreal participated in this study. Their average age and height were 25.3 + 4.1 years and 1.77 f 0.057 m respectively, while their average mass was 80.6 + 13.8 kg. Subjects had no previous history of orthopaedic or neuromuscular diseases nor recent injuries which could affect their walking pattern. None had limb length discrepancies. Subjects were right hand and leg dominant as determined from five activities, involving: (1) kicking a ball, (2) throwing a ball, (3) writing, (4) opening a jar, and (5) hopping on a single limb.

Seven body segments were defined, namely the trunk, the thighs, the shanks and the feet, by means of 24 reflective markers having a diameter of 24 mm, to identify the three-dimensional (3D) kinematics of the lower limbs. For the trunk, a marker was placed over the lateral border of the shoulders, while markers placed over the anterior superior iliac spine, crest of ilum and the greater trochanter defined the pelvis. Markers were also put over the upper anterior and mid-lateral sides of the thigh, and others covered the head of the lateral epicondyle, and the mid- and lower lateral sides of the shank. The feet were defined by three markers placed over the lateral malleolus, the heel and the lateral border of the fifth metatarso-phalangeal joint. Transformation measure- ments were taken between the external markers and the estimated joint center of rotation, to express the gait parameters in the joint coordinate system.

Data collection was performed by means of an eight-camera video system (Expert Vision 3D system; Motion Analysis Corporation, Santa Rosa, Califor- nia) and two AMTI force plates (Advanced Mechanical Technology, Inc., Newton, Massachusetts). Four cameras were placed on each side of the subject, at an average distance of 4.5 m along an arc of about 120 degrees, to cover two

246 H. Sadeghi et al./ Human Movement Science 16 (1997) 243-258

consecutive strides. Force plates were located in the middle portion of a 13 m walkway. They were 150 mm from each other, to enable the subject to take one step on each of them.

The subject were wearing comfortable attire, including shorts and running shoes. After camera calibration, they were asked to walk at a self-determined pace along the walkway and step consecutively on each force plate. This procedure was repeated until two other good trials were obtained. A trial was rejected if the subject did not take a step in the vicinity of each force plate’s center. The video data were recorded at 90 Hz while the synchronized force data were sampled at 360 Hz.

The Direct Linear Transformation was used in the Motion Analysis Expert Vision software to reconstruct the image markers into three-dimensional coordi- nates. Noise in video and force data was reduced by means of a fourth order zero-phase lag Butterworth filter, having a cut-off frequencies of 6 Hz and 30 Hz respectively (Winter, 1990). The root mean square error of the 3-D coordi- nates was less than 5 mm.

The temporal and phasic gait parameters were determined from the force plate and video data. Initial contact and toe-off were determined from the vertical ground reaction force while the ipsilateral subsequent heel-strike was determined from video data.

The inverse dynamic analysis software, Kintrak, provided by Motion Analysis Corporation, was used to calculate the muscle moments at each joint throughout the gait cycle. Instantaneous muscle powers (P) were calculated at each joint ( j> and in each plane (k) as the product of the net muscle moment (M) and the joint angular velocity ( w>.

Pj.k = ivt,,k . Wi,k.

Joint moments and angular velocities acting in the same direction resulted in power generation, whereas power absorption was obtained when the signs were of different polarities.

The energy or work ( W> generated or absorbed at each joint (j), in each plane (k), corresponded to the area under the power curve (P). It was calculated as

Wl,k = Pj.k . dt

The muscle powers and their respective mechanical energies were normalized with respect to body mass, and expressed in W/kg, and J/kg respectively. The data were also normalized with respect to the gait cycle (GC) having a mean stance phase of 60.68 + 1.72% and 61 + 1.5 1% for the right and left limbs

H. Sadeghi et al. /Human Movement Science 16 (I 997) 243-258 247

respectively. Left swing phase began at the end of the double support, at the end of loading response of the right limb gait cycle.

The power and energy bursts were labelled according to Eng and Winter (1995). The first letter referred to the joint while the number indicated the sequence of the burst. A second letter identified the appropriate plane of motion. For example H3S corresponded to the third peak power or energy burst of the hip in the sagittal plane.

The Principal Component Analysis statistical method was used to analyze the temporal gait parameters, the peak powers and their related mechanical energies, altogether 48 discrete values for each limb and for each trial. Based on the Kaiser criterion (Kaiser, 19601, factors with eigenvalues greater than one were retained and the Principal Components (PCs> which contained at least 60% of the information were kept (Statistica for window, 1994, StatSoft Technical Support by StatSoft, Inc., Tulsa). The Direct Varimax method was applied to categorize the PCs according to the magnitude of each correlation coefficient. Then within each of the extracted PCs, the parameters having a factor loading (which represents the correlation coefficient between each item and its PC) of 0.6 and above were compared by means of Student’s paired r-test ( p < 0.09, to determine the significant differences between the right and left limbs.

3. Results and discussion

Temporal and phasic gait parameters are given in Table 1. The average walking speed (1.3 1 m/s), stride length (1.46 m) and cadence (107 steps/min) for both limbs were comparable to those published in the literature (Craik, 1995; Oberg et al., 1993) for natural walking.

The mean power curves developed at the hip, knee and ankle for the right and left limbs are presented in Fig. 1 and Fig. 2 respectively. These power patterns

Table I Temporal and phasic gait parameters of 19 able-bodied individuals

Right limb

Mean

Left limb

Mean o

Speed (m/s) 1.30 0.12 1.32 0.10

Stride length (m) 1.45 0.07 1.47 0.07

Cadence (steps/min) 106.5 7.03 107.9 7.99

Stance (%) 60.7 1.72 60.9 1.50

248 H. Sadeghi et al. /Human Movement Science 16 (19971243-258

H. Sadeghi et al./Human Movement Science 16 (1997) 243-258 249

4- AZS :

B - ;

5 3

2-

g

I-

5

A15

-2 L I I I I, 0 10 20 30 40 50 60 70 80 90 100

Gait cycle (X)

Fig. 1. Powers developed at the right (a) hip, (b) knee and (c) ankle, during natural speed walking in 19

able-bodied subjects. The vertical lines indicate the begining and the end of the double support period.

have been discussed by Allard et al. (1996). Peak powers developed or absorbed in the sagittal plane were in agreement with those reported by Eng and Winter (1995) and Loizeau et al. (1995). Differences with respect to published values were noted for the peak powers in the frontal and transverse planes. This variability can be accounted for in part by the polarity of the joint moments (Crowninshield et al., 1978; Kadaba et al., 1989; Apkarian et al., 1989). Allard et al. (1996) alluded to presence of different able-bodied gait patterns.

The first four extracted Principal Components accounted for about 60% of the observations found in the right and left limbs. For each PC, the parameters having a factor loading of 0.60 and above are reported in Table 2, and grouped according to whether they were common to both limbs or related to either the right or left limb. These gait parameters were mostly related to hip and knee activities.

250 H. Sadeghi et al. /Human Morrment Science 16 (1997) 243-258

-0.2

-0 3 t

H. Sadeghi et al. /Human Movement Science 16 (1997) 243-258 251

0.3

r 0.2 r

-0.3 L

4- A25

3- >?

m

2 2-

p l- * 5 0

?I -1 -

AIS -2' I 1 / / /

0 10 20 30 40 50 60 70 80 90 iO0 110

Gait cycie (%)

Fig. 2. Powers developed at the left (a) hip, (b) knee and Cc) ankle, during natural speed walking in 19

able-bodied subjects. The left limb gait cycle is overlaid on right limb gait cycle, and begins at the 11% mark.

The HlS and K3T bursts were the only common parameters to both limbs. The HlS generation burst was associated with the control of the trunk and the collapse of the stance limb (Eng and Winter, 1995) as well as to forward progression (Allard et al., 1996). This occurred as the thigh extended at 12% of the gait cycle (GC). Both limbs generated about the same amount of peak powers and energies.

The K3T power burst which occurred at 55% GC was associated by Allard et al. (1996) with an internal rotation of the thigh during push-off, in moving the body center of mass towards the contralateral limb. Both limbs developed the same peak powers.

252 H. Sadeghi et al./Human Movement Science 16 (1997) 243-258

Table 2

Peak powers and energies common to both limbs and to the right and left limbs

Power (W/kg)

Right limb

Mean 0

Energy (J/kg lo-‘)

Left limb Right limb Left limb

Mean u Mean u Mean IJ

Both limbs

HlS 1.50 1.10 I .23

K3T 0.07 0.07 0.05

Right limb

H3S 3.02 * 1.42 2.40 ’ H3F -0.19 0.14 - 0.22 H2T - _ -

KlS - _ _

L.eji limb

HlF -0.81 0.33 - 0.95

HIT -0.18 0.13 -0.17

K2S 0.45 * 0.36 0.56 * K3S - - -

KlF -0.12 * 0.27 0.11 * K2T -0.12 * 0.08 -0.07 *

K3T 0.07 0.08 0.05

0.99 17.10 17.50 24.20 22.60 0.16 _ - _ _

1.53 29.60 * 17.90 17.30 * 9.50 0.29 _ - _ _

- 5.32 3.90 5.00 4.00

_ - 4.80 3.00 - 4.40 3.90

0.57 - 16.50 * 8.00 -20.50 * 16.10

0.17 - 1.57 1.50 - 1.70 2.40

0.53 4.90 3.90 5.30 5.40

13.90 ’ _ - 8.30 -5.30 * 0.04

0.16 -0.90 * 2.50 0.90 * 1.50

0.10 -0.90 * 0.60 -0.60 * 0.70

0.16 0.40 0.50 0.40 1.10

* p < 0.05

The factor loading of the muscle powers and mechanical energies of the right limb are presented in Fig. 3. Including the common HIS and K3T values, four peak powers and four energy bursts characterized the right limb. Most of the peak powers occurred in the sagittal plane, although transverse and frontal powers and energies were also present. All but KlS and H3F were generating. Most of the peak powers and energies occurred at the hip, followed by some at the knee. Though significant differences were reported between sides in the ankle energies (Allard et al., 19961, this parameters did not appear in the factor analysis. The PCA analysis revealed also that the most important gait parameters of the right limb were related to propulsion. The H3S, H3F and K3T power bursts occurred essentially during the push-off period. Right limb values were generally the highest, although only the H3S activity was significantly different ( p < 0.05).

Seven peak powers and eight energy bursts characterized the left limb, as shown in Fig. 4. The peak powers did not occur principally in the sagittal plane as for the right limb, but rather involved all three planes. There was as much absorption as generation, and most of the activity occurred at the knee. This

H. Sadeghi et al. / Human Movement Science 16 (1997) 243-258

0.75

d

ii,.,

0.25

-0.75

t

253

-1 1 HlS_P HIS-E HJS_P H3S_E HJF_P H2T_E KlS_E KJT_P

Fig. 3. Factor loading of the peak powers and mechanical energies of the right limb.

activity was spread throughout the stance phase, rather than being concentrated in a specific period of the gait cycle. The left limb had significantly higher values for HlF, K2S and KlF, while the right limb generated more K3S energy.

Generally, the PCA has identified both the peak powers and their respective energies to characterize the biomechanical behaviour of the lower limbs. Most

1

0.7s

d ‘si L 0.5

B 0.25

0

4.2s

5 P 4 .Q.5

4.75

HlS_P HI F-P HIT-P HlS_E Hl F-E

KZS_P W_E K1F_E KZT_E KS_E HIT-E KzS_E Kl F-P KZT_P UT_P

Fig. 4. Factor loading of the peak powers and mechanical energies of the left limb.

254 H. Sadeghi et al. /Human Movement Science 16 (1997) 243-258

often, significant differences between the lower limb values were noted for both types of parameters.

Targeting a force plate during a gait assessment does not significantly affect the ground reaction forces (Grabiner et al., 1995), but awareness by subject to take consecutive steps on each force plate during data collection may have had an influence. Furthermore, the subjects always stepped on the first platform with their right foot. This had the advantage of having the largest number of trials for that single condition but at the cost of increasing the chances of obtaining gait asymmetry. Our subjects were evaluated with their arms crossed over the chest, to avoid occlusion of the pelvis and hip markers. This may have influenced our results, since asymmetrical arm action has the potential to compensate for asymmetries elsewhere in the body (Hinrichs, 1992).

Furthermore, the relative displacements of the markers due to soft tissue motion were not corrected by a solidification process (Cheze et al., 1995). Also, the mechanical energies were calculated at each joint and for each plane from the respective muscle powers, although powers and energies are scalar terms. Nonetheless, this method was used by Eng and Winter (19951, as well as Allard et al. (1996), to describe able-bodied gait, and Loizeau et al. (1995) applied it to study patients fitted with total hip prostheses.

The muscle powers and mechanical energies determined from the Principal Component Analysis will be discussed with respect to each limb, and then in term of asymmetry.

3.1. Right limb

Our results bring further evidence for the importance of sagittal and frontal plane actions during gait (Winter, 1990; Mackinnon and Winter, 19931, espe- cially for those occurring at the hip (Olney et al., 1994; Eng and Winter, 1995).

The right limb generated the greatest powers and energies in the sagittal plane, and most of their actions were developed during the push-off period. This propulsion began with the right ankle plantarflexing (A2S = 3.21 W/kg) at 53% of the gait cycle (GC), followed rapidly by a strong pull at the hip due to an H3S generation (3.02 W/kg) at 58% GC. The hip pulled the thigh forward and controlled the collapse of the pelvis on the contralateral limb (H3F = - 0.19 W/kg). While the ankle pushed and the hip pulled, the right knee adjusted itself to ensure a good push-off. It flexed under the extension moment (K3S = - 0.14 W/kg) and externally rotated (K3T = 0.07 W/kg), due to the ankle everting motion.

H. Sadeghi et al./Human Mocement Science 16 (19971243-258 255

The other hip (Hl S and H2T) and knee (KlS) actions were spread throughout

the midstance period, extending from about 8% to 45% of the gait cycle. Considering that they occurred during the contralateral limb swing phase and due to their distant functional association, these powers appeared to be related to some form of support function. For example, HlS was associated with to the control of trunk advancement (Eng and Winter, 1995), KlS controlled knee collapse (Winter, 19911, while H2T can cause the thigh to go into external rotation in preparation for the contralateral heel-strike.

Only the H3S power and its energy burst were significantly different. The asymmetry occurred in the push-off period, denoting a 20.6% stronger pulling action of the right hip. Interestingly, the right limb had a slightly faster walking speed than that of the left side. Olney et al. (1994) explained that peak ankle and hip powers at push-off were the most useful parameters in predicting stride speed, for the unaffected limb of subjects with hemiplegia. Based on these observations, as well as the concentration in the push-off period of most PCA factors, and the identification of many muscle power generation bursts, we therefore assume that this limb’s main function was that of propulsion, with a secondary action of support, occurring during midstance.

3.2. Left limb

The left limb was characterized by a series of power and energy absorption and generation peaks spread throughout the entire stance phase. These muscle activities occurred in all three planes, and not mainly in the sagittal plane as for the right limb.

At heel-strike, the hip was essentially active in (a) controlling trunk forward motion, (b) contributing to the forward propulsion by its HlS generation (1.23 W/kg), (c) controlling the trunk rotation by its HlT absorption (0.02 W/kg), and (d) supporting the pelvis list on the contralateral side (HlF = -O.lOW/kg). During midstance and push-off, the knee provided a series of gait adjustments. For example, the K2S power burst was restoring knee extension after its initial flexion at the end of heel-strike and the K3S absorption peak compensated for the hip pulling action and the ankle propulsion.

Because of the controlling action of the hip during midstance and the known passive role of the knee at push off, this limb had mostly a function of support. This was characterized by three strong controlling actions (HlF, KlF and K2S). A significantly lower K3S power absorption was attributed to the reduction of the knee action during push-off, in maintaining a walking speed similar to that of the right limb.

256 H. Sadeghi et al./Humn Movement Science I6 (1997) 243-258

3.3. Limb asymmetry

This 3-D simultaneous bilateral gait study supports previous studies (Arsenault et al., 1986; Herzog et al., 1989; Rosenrot et al., 1980) where asymmetry was documented. Our results, and those of Gunderson et al. (19891, challenge the practice of conducting unilateral limbs evaluations, or pooling right and left limb gait data. Gait asymmetry in able-bodied subjects should not be considered as a pathological phenomenon, but interpreted in terms of control and propulsion strategies (Hirasawa, 1981; Hirokawa, 1989). However, no one has yet specified which gait parameters were associated with each of these strategies.

Five parameters were shown to be significantly different between the limbs. For the left limb, these occurred during heel-strike (HlF), midstance (KlF, K2S) and push-off (K3S), with the later being an absorption burst. These were explained in terms of control or stabilising actions. For the right limb, there was only the H3S generating burst which occurred during push-off, delineating a propulsion function.

These results must interpreted with caution, since our subjects were all right-handed and right-footed. The functional asymmetries might reflect limb dominance of the subjects. Gunderson et al. (1989) and Yang and Winter (1985) pointed out that averaging data across subjects tends to increase symmetry. Lack of asymmetry may be explained in part by the choice of the of the proper gait parameter. Gunderson et al. (1989) used temporal and phasic gait parameters as well as joint angles to quantify gait asymmetry. Hannah et al. (1984) concluded from kinematic data that able-bodied subjects walked with reasonable symmetry. However, Herzog et al. (1989) found gait asymmetries in force plate data to be much larger than expected for a normal population. We have selected muscle power and mechanical energies, because they group both kinetic and kinematic parameters, and these have been found by others (Olney et al., 1994; Loizeau et al., 1995) to be related to clinical findings.

4. Conclusion

The results supported the idea of a functional gait asymmetry. For the limb which had a propulsion function, characterized by a strong H3S burst, most of the parameters identified by the PCA were associated with the hip and knee. These were concentrated during the push-off period. There was a secondary support function which occurred during midstance. For the limb having a supporting function, most of its activities were associated with the knee, and

H. Sadeghi et al. / Human Movement Science 16 (1997) 243-258 251

these were spread throughout the stance phase. None of them was associated with propulsion.

Acknowledgements

This work was funded in part by the Ministere de l’Industrie, du Commerce, des Sciences et de la Technologie of Quebec (Programme Synergie), the Natural Sciences and Engineering Council of Canada and Les laboratoires d’ortheses et de protheses Medicus. The authors would like to thank the Ministry of the Cultural and Higher Education and the Tarbiat Moallem University for their financial support to Heydar Sadeghi.

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