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Kinematic correlates of walking cadence in the foot
Journal of Biomechanics 43 (2010) 2425–2433
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Kinematic correlates of walking cadence in the foot Paolo Caravaggi a,n, Alberto Leardini b,1, Robin Crompton a,2 a b
HACB, School of Biomedical Sciences, University of Liverpool, Sherrington Buildings, Liverpool L69 3GE, UK Movement Analysis Laboratory, Istituto Ortopedico Rizzoli, Bologna, Italy
a r t i c l e in fo
abstract
Article history: Accepted 9 April 2010
Evidence has frequently been reported of modifications in gait patterns within the lower limb related to the cadence of walking. Most reports have concerned relationships between cadence and kinematic and the kinetic changes occurring in the main joints and muscles of the lower limb as a whole. The aim of the present study was to assess whether significant changes are also measurable in kinematics of the foot segments. An existing 15 marker-set protocol allowed a four-segment foot and shank model to be defined for relative rotations between the segments to be calculated. Stereophotogrammetry was employed to record marker position data from ten subjects walking at three cadences. The slow- and normal cadence datasets showed similar profiles of joint rotation in three anatomical planes, but significant differences were found between these and the fast cadence. At all joints, frame-by-frame statistical analysis revealed increased dorsiflexion from heel-strike to midstance (po 0.05) and increased plantarflexion from midstance to toe-off (po 0.05) with increasing cadence. From foot-flat to heel-rise, the fast cadence kinematic data showed a decreased range of motion in the sagittal-plane between forefoot and rearfoot (3.21 7 1.21 at slow cadence; 2.01 7 0.81 at fast cadence; p o 0.05). The cadences imposed and the multisegment protocol revealed significant kinematic changes in the joints of the foot during barefoot walking. & 2010 Elsevier Ltd. All rights reserved.
Keywords: Multisegment foot kinematics Joints of the foot Motion analysis
1. Introduction Over the last decade it has become apparent that reduction of the foot to a single segment oversimplifies its role in lower limb dynamics during gait. The pioneering work of Lundberg et al. (1989a,b,c), using roentgenographic analysis, stimulated interest in the investigation of motion occurring at the internal joints of the foot (DeLozier et al., 1991; Scott and Winter, 1991; D’Andrea et al., 1993). The outcome of these studies and advances in stereophotogrammetric technique have motivated researchers to design non-invasive surface marker protocols to measure internal joint motion in the foot, for clinical and general biomechanical investigations, in order to provide a more detailed description of the foot’s complex kinematics. Two- (Rattanaprasert et al., 1999; Hunt et al., 2001), three- (Kidder et al., 1996; Carson et al., 2001) and four-segment (Leardini et al., 1999; Leardini et al., 2007) three-dimensional rigid-body models of the foot have been proposed. These have indeed revealed that skin-mounted markers can consistently, and with a good degree of repeatability, detect significant amounts of motion at the major joints in all three
n
Corresponding author. Tel.: + 44 151 794 6867; fax: + 44 151 794 5517. E-mail addresses: [email protected] (P. Caravaggi), [email protected] (A. Leardini), [email protected] (R. Crompton). 1 Tel.: + 39 051 6366522; fax: + 39 051 6366561. 2 Tel.: + 44 151 794 5456; fax: +44 151 794 5517. 0021-9290/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2010.04.015
anatomical planes. Moreover, mean differences between joint rotation data derived from tracking bone-pins and skin markers have been reported to be greater than 31 in only 35% of the kinematic data during stance (Nester et al., 2007). However, a lack of standardization in the definition of neutral angles between the segments, in the bony landmarks employed, in the definition of local reference frames and scarcity and/or non-uniformity of published data make comparison of the results from different studies difficult. An attempt to compare the ranges of motion and the temporal profiles of rotation angles between different multisegment foot models (Benedetti et al., 2008) concluded that only rotations in the sagittal-plane at the rearfoot and at the first metatarsophalangeal joint were consistently reproduced by different methodologies. Although walking speed has been shown to affect the kinematics and kinetics in the lower limbs (Murray et al., 1984; Kirtley et al., 1985), if, and where, any walking-speed-related modifications also occur in the foot has not been fully addressed. The inference that significant kinematic changes must occur along the longitudinal arch of the foot when walking at faster gaits finds support in early pedobarographic studies (Clarke, 1980; Cavanagh and Rodgers, 1985; Rosenbaum et al., 1994), and more recently in an application of a novel technique to assess differences in pressure records (Pataky et al., 2008), which revealed that midfoot and proximal forefoot peak plantar pressures are negatively correlated with walking speed. To the best of the authors’ knowledge, only
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one study has tried to assess the influence of walking speed on foot kinematics (Tulchin et al., 2009). In that study, however, the marker protocol employed did not allow for any tracking of the midfoot and only sagittal-plane rotations were reported. Therefore, for the present study, a more complete foot protocol (Leardini et al., 2007) was chosen, based on a clear definition of the bony landmarks and of the local reference frames and designed to meet the recommendations of the International Society of Biomechanics (Wu et al., 2002).
From a clinical perspective, a study of the influence of walking speed on foot kinematics would allow clinicians to take account of possible speed-related kinematic modifications when employing multisegment models to assess the alterations occurring at the main joints of the foot pre- and post-operatively, or to evaluate the overall effects of treatments. In fact progression speed frequently cannot be controlled in clinical gait analysis, and therefore the possibility of influence by established speed-related biases should be considered during clinical interpretation. Consequently, the main goal of this investigation was to test if significant kinematic changes do occur between foot segments when walking at different speeds. For this purpose, we adopted the skin-mounted marker protocol devised by Leardini et al. (2007), which allows tracking of the six degrees-of-freedom motion of the shank, calcaneus, midfoot and metatarsal segments.
2. Methods
Fig. 1. The reflective markers attached to the lower limb and foot of one of the subjects who volunteered in the study.
A six-camera motion capture system set to 250 Hz (ProReflex 1000 MCU, Qualysis, Gothenburg, Sweden) was employed to collect marker trajectories for the foot segment kinematics analysis. Ten healthy young male subjects (age 29.37 6.4 yrs; height 178.8 76.0 cm and weight 73.8 78.7 Kg) with no history of lower limb main injuries nor gross musculoskeletal abnormalities of the lower limb (two subjects had relatively low-arched feet) were analysed during walking on a 6 m long wooden walkway. Simultaneously, a Kistler force platform (model 9281C, Kistler Instruments Ltd., Hook, Hampshire, UK) recorded ground reaction force (GRF) at 500 Hz. The left shank and foot of each subject were instrumented with fifteen 7 mm diameter reflective markers, attached to the skin with doublesided adhesive tape (Fig. 1), according to Leardini et al. (2007). Before starting the walking trials, in order to define the neutral position of the foot, a 1 s static acquisition was taken with the subject standing still in a right-leg support (Caravaggi et al., 2009), the left foot in contact with the floor but with minimum load, i.e. no-weight bearing for the analysed leg. Each subject was then asked to walk at three subjectively determined cadences: normal, slow and fast. Slow and fast speeds were described to the subjects as the slowest and the fastest natural gaits that they could reproducibly achieve. In order to minimize intra-subject speed variability, and before starting data acquisition, each subject was requested to practice the different gait speeds until he felt comfortable in reproducing each walking speed. Ten walking trials were recorded for each subject at each of the three cadences. Triplanar intersegment rotations for the shank/calcaneus, calcaneus/midfoot, midfoot/metatarsus and calcaneus/metatarsus joints were calculated (Grood and Suntay, 1983; Leardini et al., 2007) to derive dorsiflexion/plantarflexion, eversion/inversion and abduction/adduction, respectively in the sagittal, frontal and transverse planes. Frame-by-frame statistical differences between time-histories of the rotations in each sample within the normalized stance phase duration and between the relevant ranges of
1.2 1.1
Stance duration [s]
1 0.9 0.8 0.7 0.6 0.5 0.4
slow
normal
fast
Cadence group Fig. 2. Stance phase durations across 100 trials per walking cadence group (slow, normal and fast).
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duration across the 100 trials per cadence group are plotted for each trial/subject/cadence combination in Fig. 2. Inter-subject means (7standard deviation) of stance phase duration were 0.834 s ( 70.097 s), 0.652 s (70.068 s) and 0.533 s ( 70.046 s), respectively for the slow, normal and fast cadences. The estimated inter-subject means (7standard deviations) of cadence (steps/min) were 88.1 ( 710.3), 110.1 ( 711.3) and 130.2 ( 711.0), respectively for the slow, normal and fast cadence sets. A clear trend of longer stance duration for slower cadence can be detected, though associated also with larger inter-subject variability. In agreement with previous findings (Andriacchi et al., 1977; Nilsson and Thorstensson, 1989), analysis of the GRF revealed that increasing cadence was accompanied by higher peaks within the time-histories of the three GRF components (Fig. 3). This was especially true for the first two peaks of the vertical component, i.e. in early- (1.0270.07BW in slow walking; 1.4070.13BW in fast walking: p o0.001) and mid-stance (0.85 70.05BW in slow walking; 0.4970.01BW in fast walking: po0.001), and for the two peaks of the anterior–posterior component in early(0.1470.03BW in slow walking; 0.2970.06BW in fast walking: po0.001) and late-stance (0.17 70.02BW in slow walking; 0.2570.05BW in fast walking: p o0.001). Slow- and normal cadence sets displayed similar rotation profiles, but differences, however, existed between these two groups on the one hand and fast walking on the other hand (Fig. 4). Kinematic data from the normal walking group are largely in agreement with the report of Leardini et al. (2007), the only evident difference being in sagittal-plane rotation between calcaneus and midfoot (Fig. 5, top). The inter-trial variability, averaged over stance duration, of joint rotations for 10 repetitions from the same subject, and for one walking cadence, was between 70.31 and 71.01, the sagittal-plane rotation between shank and calcaneus showing the largest variability, most likely because of the correspondingly large range. Frame-by-frame statistical analyses performed separately for each sample of the rotation time-histories in the three anatomical planes from slow- and fastcadence groups are shown in Fig. 6, and are commented upon individually in the following subsections. Where not explicitly reported, the results presented below should be considered to be statistically significant at 95% confidence level.
3.1. Effect of cadence on sagittal-plane motion
Fig. 3. Inter-subject mean temporal profiles of ground reaction forces across 10 subjects and 100 trials at three walking cadences. From top to bottom: vertical GRF; anterior–posterior GRF and medio-lateral GRF. Positive GRF are directed upwards, anteriorly and medially, respectively. motion (ROM) for different walking speeds were tested using the non-parametric Mann–Whitney U-test (Mann and Whitney, 1947). From the measured stance duration, cadence was estimated according to the values of the gait cycle durations calculated from the correlation between the stance interval as percentage of the gait cycle and the walking speed (Kirtley et al. (1985). Average walking speed associated with the three cadences was taken from a previous work (Pataky et al., 2008).
3. Results Three (slow, normal and fast) different, and consistent, mean patterns of walking were obtained. The values of stance phase
For all joints, increased cadence appeared to modify the pattern of rotation in the sagittal-plane in two contrasting ways at different stance phases: by increasing dorsiflexion from around heel-strike to midstance; and by increasing plantarflexion from around midstance to toe-off (Fig. 6). The midtarsal joint was more dorsiflexed from around 5% to 40% of stance and more plantarflexed from around 60% to 100% of stance when comparing the fast- to the slow cadence sets.
3.2. Effect of cadence on frontal plane motion With increase in the cadence, the calcaneus was found to be more inverted with respect to the shank from around midstance to push-off (around 80% of stance); but more everted just before toe-off (Fig. 6). Similarly, the midfoot segment was more inverted with reference to the calcaneus from midstance to push-off. The metatarsus was more inverted with reference to the calcaneus up to midstance; but more everted during late stance, albeit for a shorter period.
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Fig. 4. Left to right: mean temporal profiles of the rotation angles between: shank and calcaneus; calcaneus and midfoot; midfoot and metatarsus and calcaneus and metatarsus across 10 subjects and 100 trials at three walking cadences during normalized stance phase. From top to bottom: dorsiflexion/plantarflexion; eversion/inversion and abduction/adduction.
Fig. 5. Mean temporal profiles (7 1 SD) of the three rotation angles between calcaneus and midfoot across 10 subjects and 100 trials at normal cadence during normalized stance phase. From top to bottom: dorsiflexion/plantarflexion; eversion/inversion and abduction/adduction.
3.3. Effect of cadence on transverse plane motion The calcaneus was more adducted with reference to the shank during late stance. The midfoot was more abducted with reference to the calcaneus up to midstance; but more adducted around push-off, albeit for a shorter period (Fig. 6). During two relatively short phases, just prior to and just after midstance, the metatarsus was, respectively, more adducted and more abducted with reference to the midfoot. The metatarsus was more adducted with reference to the calcaneus from around midstance to pushoff.
3.4. Analysis of the range of motion Analysis of the triplanar joint ROM confirmed the inference from visual inspection of the mean temporal profiles of the
2429 Fig. 6. In black, time-normalized intervals of those rotation angles statistically different between slow and fast walking cadences at 95% confidence interval. From top to bottom: comparison of joint rotations in the sagittal, frontal and transverse planes. From left to right, between: shank and calcaneus; calcaneus and midfoot; midfoot and metatarsus and calcaneus and metatarsus. (e.g. for sagittal-plane rotations) Positive (+1) ranges designate greater dorsiflexion at fast cadence; negative ( 1) ranges designate greater plantarflexion at fast cadence and zero ranges designate sagittal-plane rotation angles not statistically different between slow and fast cadences.
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Table 1 Triplanar range of motion values [deg] between shank and calcaneus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
6.7 3.6 1.1 3.5 1.0 0.8 11.5 2.9 3.0 6.4 1.9 2.1 11.6 2.1 2.7 21.6 6.2 6.1 5.2 1.2 1.7
6.9 3.3 0.9 3.6 0.8 0.6 10.8 2.6 2.4 6.6 2.1 1.9 11.4 2.1 2.2 22.1 5.9 5.4 5.3 1.0 1.5
1.8 1.4 0.7 1.2 0.8 0.6 3.7 1.1 1.9 2.6 1.0 1.4 4.0 0.9 1.7 6.6 1.9 3.4 1.9 0.7 0.9
6.7 4.2 1.2 4.1 0.9 0.8 9.8 2.9 2.8 7.1 1.9 2.2 11.1 2.5 2.7 22.2 6.3 6.3 6.2 1.4 1.8
6.7 4.1 1.1 4.0 0.6 0.6 8.8 2.7 2.0 6.9 1.7 1.9 10.9 2.4 2.2 21.9 5.9 6.2 6.0 1.3 1.4
1.6 1.7 0.7 1.1 0.8 0.5 3.9 1.2 1.8 2.9 0.9 1.4 3.5 1.3 1.5 7.0 1.8 3.5 2.4 0.8 1.1
6.7 4.3 1.4 4.9 0.9 0.8 7.5 2.8 2.9 7.6 1.5 2.2 8.5 2.3 2.0 22.8 6.2 6.4 6.4 1.6 1.8
6.7 4.3 1.0 5.1 0.5 0.6 7.2 2.7 2.4 7.2 1.3 1.8 7.8 2.2 1.9 22.4 5.8 5.9 6.1 1.5 1.3
2.1 2.0 1.1 1.6 1.0 0.5 2.9 1.2 1.8 2.4 0.9 1.5 2.8 1.6 1.2 5.8 1.7 3.6 2.4 0.9 1.5
p1
p2
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p3
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Table 2 Triplanar range of motion values [deg] between calcaneus and midfoot during seven phases of stance and for three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
p1
p2
p3
1.5 1.7 1.3 0.9 1.8 0.7 7.1 3.1 1.9 3.9 2.2 2.0 5.6 1.6 2.0 10.9 7.1 5.4 2.9 1.4 1.1
1.4 1.4 0.9 0.7 1.7 0.7 6.9 3.1 1.7 3.7 1.9 1.7 5.1 1.3 1.6 11.0 7.0 5.1 3.0 1.2 1.0
0.9 1.2 1.0 0.6 0.8 0.5 1.4 1.0 0.8 1.6 1.2 1.3 2.3 1.1 1.4 1.7 1.9 1.9 1.0 0.7 0.5
1.8 1.9 1.3 1.0 1.9 0.9 6.5 3.0 1.9 4.2 2.3 2.3 5.2 1.6 1.9 11.0 6.8 5.6 2.8 1.1 1.1
1.7 1.7 1.1 0.9 1.8 0.9 6.1 3.0 1.8 3.9 2.1 1.9 4.6 1.5 1.5 11.1 6.9 4.9 2.7 1.1 1.0
1.1 1.1 1.3 0.6 0.8 0.5 1.5 1.1 0.9 1.9 1.1 1.4 2.6 1.0 1.5 2.1 1.9 2.2 1.1 0.5 0.6
2.1 2.1 1.5 1.0 2.1 1.1 5.1 3.3 2.2 4.7 1.6 2.6 4.6 1.7 2.1 10.8 6.6 6.2 2.2 1.2 0.9
2.0 1.8 1.2 1.0 2.0 0.9 4.5 2.8 1.8 4.5 1.7 2.7 3.6 1.1 1.9 10.9 6.7 5.7 2.2 1.1 0.8
1.2 1.3 1.2 0.6 1.1 0.6 1.8 1.5 1.1 1.7 0.8 1.3 3.1 1.3 1.4 2.4 1.8 2.1 1.0 0.6 0.5
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rotation angles, that it was only the slow versus fast cadence comparison which displayed the evident variation (Tables 1–4). All foot joints showed increased ROM in the sagittal-plane during early stance with increasing cadence. With the exception of the midfoot/metatarsus joint, the total sagittal-plane ROM during normalized stance phase duration was unaffected by walking cadence. Analysis of the ROM in the interval between 21% and 80% of normalized stance revealed a decrease in both the
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relative sagittal-plane ROM between calcaneus and midfoot (7.1171.41 at slow cadence; 5.1171.81 at fast cadence: po0.001) and of relative sagittal-plane ROM between calcaneus and metatarsus (5.61 71.31 at slow cadence; 4.6171.61 at fast cadence: p o0.001). In contrast, during the same interval, the sagittal-plane ROM between midfoot and metatarsus increased from 3.6171.01 at slow cadence to 5.9171.81 at fast cadence (p o0.001). In the interval foot-flat to heel-rise (which covers the
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Table 3 Triplanar range of motion values [deg] between midfoot and metatarsus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
1.1 1.4 1.1 0.9 2.4 0.7 3.6 2.9 2.8 4.0 1.1 1.2 2.3 2.0 2.0 10.4 5.2 5.3 1.1 0.7 1.3
1.0 1.2 0.9 0.7 2.1 0.6 3.5 2.9 2.2 4.2 0.9 1.3 2.0 1.7 1.8 10.9 4.7 5.3 0.9 0.6 1.1
0.8 0.8 0.7 0.6 1.3 0.5 1.0 0.9 1.6 1.5 0.8 0.6 1.5 1.3 1.3 2.8 2.0 1.7 0.9 0.4 0.7
1.4 1.6 1.1 1.0 2.5 0.9 4.3 3.0 2.8 4.3 1.0 1.2 2.4 1.8 2.3 11.3 5.1 5.6 1.0 0.8 1.1
1.0 1.5 1.0 0.8 2.2 1.0 4.2 3.0 2.3 4.4 0.9 1.2 2.1 1.4 2.1 11.9 4.6 5.7 0.8 0.6 1.0
1.0 1.0 0.9 0.7 1.2 0.5 1.2 0.8 1.7 1.3 0.6 0.6 1.6 1.5 1.4 2.9 1.9 1.7 0.7 0.5 0.6
1.5 1.5 1.2 1.1 2.5 0.9 5.9 3.2 2.7 4.0 0.9 0.9 3.1 1.7 2.6 12.4 5.2 5.6 1.0 1.0 0.9
1.2 1.3 0.9 0.8 2.3 0.8 5.8 3.0 2.3 3.8 0.8 0.9 2.2 0.9 2.1 13.3 4.9 5.5 0.9 0.8 0.8
1.0 0.9 0.9 0.8 1.3 0.5 1.8 1.0 1.7 1.4 0.4 0.6 3.0 1.6 2.1 3.5 2.0 1.9 0.6 0.6 0.5
p1
p2
p3
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n
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n
n
n
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n
n
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Table 4 Triplanar range of motion values [deg] between calcaneus and metatarsus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
p1
p2
1.7 1.6 2.1 1.3 2.3 1.3 5.6 3.2 4.0 7.9 2.0 3.0 6.1 3.3 2.4 17.6 7.1 8.2 3.2 1.0 1.1
1.5 1.4 1.5 1.1 2.1 1.1 5.4 3.3 3.9 7.8 2.0 2.9 5.4 2.8 2.2 17.9 6.3 8.0 3.2 0.8 1.1
0.9 0.7 1.5 0.9 1.2 0.8 1.3 1.0 1.6 2.1 1.0 1.6 3.4 2.2 1.2 2.8 2.8 2.4 1.2 0.6 0.6
2.2 1.6 2.2 1.4 2.3 1.2 4.8 3.0 4.4 8.5 2.4 3.2 5.7 3.3 2.9 18.1 7.2 8.6 2.9 1.1 1.1
1.9 1.6 2.1 1.3 2.2 1.3 4.8 2.9 4.1 8.1 2.3 2.9 5.2 2.3 2.5 18.2 6.6 8.9 3.0 0.9 1.0
1.1 0.8 1.3 1.0 1.2 0.6 1.1 0.9 1.9 2.1 1.2 1.7 3.0 2.4 1.5 2.6 2.8 2.9 0.9 0.7 0.6
2.5 1.8 2.1 1.5 2.3 1.6 4.6 2.6 4.9 8.5 3.0 2.2 4.4 3.1 2.9 18.0 8.1 7.9 2.0 1.2 1.1
2.0 1.6 2.0 1.2 2.2 1.6 4.5 2.6 4.5 8.3 3.3 2.2 3.4 2.5 3.0 17.8 7.4 7.5 2.0 1.1 0.9
1.3 1.2 1.2 1.2 1.2 0.9 1.6 0.9 2.3 1.8 1.4 1.3 2.8 2.3 1.8 3.4 3.1 2.9 0.8 0.6 0.7
n
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part of the stance phase during which the whole sole of the foot is in contact with the ground), the sagittal-plane ROM between foot joints was either unaffected by, or decreased with cadence.
4. Discussion Prior to this study, because of the small degree of motion at the joints of the foot, and due to the limited techniques utilised, it had not yet been fully established whether significant kinematic
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changes occur at the foot joints between different walking cadences. A carefully configured stereophotogrammetric system with six cameras and a recently established multisegment protocol with 15 markers were exploited over ten normal subjects to identify the possible alterations in ground reaction force and in the rotations at four main foot joints during the stance phase of barefoot walking at three self-determined cadences. Frame-byframe statistical analysis revealed interesting differences. Analysis of the mean kinematics profiles (Fig. 4) and of the ROM (Tables 1 to 4) revealed that most joint motion occurred in
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the sagittal-plane but cadence appeared to significantly affect rotations in all three anatomical planes. The continuity and lengths of the time-normalized intervals (Fig. 6) indicate that increase in the cadence systematically affects joint kinematics in the foot. The pattern of cadence-dependent joint kinematic changes in the sagittal-plane was clearly distinct in early and late phases: increased segment dorsiflexion up to around midstance, but increased segment plantarflexion from midstance to toe-off (Fig. 6, top plots). In the frontal plane, in general, increased cadence seemed correlated with greater inversion between foot segments (Fig. 6, middle plots).The statistical analysis showed that both the midtarsal joint, between calcaneus and midfoot, and the tarsometatarsal joint, between midfoot and metatarsus, appeared to be involved in absorbing the vertical forces arising during early stance (Fig. 4 and Fig. 6, from around 5% to 40% for the midtarsal joint). This appears to be a consequence of the higher vertical impact on the foot in early stance with increasing walking speed (Fig. 3, top plot), which acts to increase joint dorsiflexion. However, in accordance with the sequence of kinematic events at the rearfoot, the tarsometatarsal joint appears to contribute to absorbing the vertical component of the GRF only later, from around 20% of the stance (during foot-flat). While the tarsometatarsal joint maintained a slightly dorsiflexed position until heel-rise, the midfoot continued dorsiflexing until push-off (around 80% of stance). Higher mobility of the midtarsal joint in the sagittal-plane finds confirmation in the analysis of its ROM in the interval 21%–80% of stance, which for the normal cadence set, for example, showed a total value of 6.5171.51 (Table 2) and for the metatarsus relative to the midfoot of 4.3171.21 (Table 3). Our kinematic data are in agreement with Tulchin et al. (2009) in showing that hindfoot and forefoot display a clear shift towards plantarflexion with increasing walking cadence. However, the detailed frame-by-frame statistical analysis of the present investigation allows clear identification of when, and where, these cadence-dependent kinematic changes occur. Moreover, some major kinematic changes were also recorded in the frontal and the transverse planes, despite their limited motion and despite the fact that the skin motion errors, which intrinsically affect these measurements, might have been expected to have prevented identification of patterns as clear as those which were observed in the sagittal-plane. A further addition to the finding of Tulchin et al. (2009) is that the chosen marker-set allowed for a midfoot segment to be analysed, which permitted estimation of the individual contributions of midtarsal and tarsometatarsal joints to longitudinal arch deformation. Analysis of the joint ROM in the interval foot-flat to heel-rise revealed either decreased or unaffected sagittal-plane motion between foot segments with increasing walking cadence. Decreased vertical GRF at higher cadences in the central part of stance (Fig. 3) could certainly contribute to apparent archstiffening but cannot alone provide an explanation for increased plantarflexion from midstance until toe-off (Fig. 6). It therefore seems sensible to consider a possible active contribution to archaugmentation from the intrinsic muscles of the foot. The timing of activity onset of the intrinsic muscles, which work in synergy, as a functional unit, to support the medial longitudinal arch (Mann and Inman, 1964), appears well correlated with the pattern of plantarflexion identified in this investigation. Therefore, the combined action of the windlass mechanism (Hicks, 1954) and of the arch-supporting intrinsic and extrinsic muscles, such as the tibialis posterior, the activities of which are likely to increase with increasing walking speed (Hof et al., 2002; Neptune and Sasaki, 2005), can not only act to restrain segment dorsiflexion at midstance but also to increase the segment plantarflexion in late stance. The present detailed kinematic analysis of the foot joints supports the inference of some manner of arch-stiffening
mechanism at increasing walking cadence, as recently highlighted by pedobarographic analysis (Pataky et al., 2008). Most of the mean temporal profiles of the rotation angles for the normal walking group (Fig. 4) proved similar to those reported by Leardini et al. (2007). The most evident differences were in the larger sagittal-plane motion found between the calcaneus and midfoot segments and in the less pronounced eversion found between the midfoot and metatarsus during late stance in the present study. In contrast to Leardini et al. (2007), this study revealed a clear pattern of dorsiflexion between calcaneus and midfoot lasting until late stance, and subsequent plantarflexion at toe-off (Fig. 5, top), a pattern of motion more in agreement with the findings of Nester et al. (2007) who reported temporal profiles of sagittal-plane rotation, between calcaneus and navicular, and between calcaneus and cuboid, very similar to that between calcaneus and midfoot in the present study. Further, the total ROM of 8.6173.11 between those joints reported by Nester et al. (2007), was only slightly lower than that measured in this study (10.91 71.71, see Table 2). The discrepancies highlighted above could be the consequence of differences in the populations and/or the results of the sensitivity of the protocol to minor differences/ errors in the localization of the bony landmarks and relevant marker attachment. An existing foot and shank gait analysis protocol enabled careful assessment of the kinematic changes occurring in the joints of the foot when walking at three different cadences. These consistently affected rotations at the ankle, midtarsal and tarsometatarsal joints; i.e. increased cadence resulted in increased dorsiflexion in early stance and increased plantarflexion in late stance, accompanied also by a general increase in inversion. Since walking cadence has significant effects on foot kinematics, a direct implication of this study for clinical practice is that, whenever possible, walking cadence should be controlled and reported together with kinematic data. It is essential that kinematic variations due to foot pathologies or following surgery can be properly assessed in relation to the altered walking speed of the subject. Finally, the detailed analysis of the ROM revealed that, during midstance, increased cadence is related to restricted sagittalplane motion at the midtarsal joint and, more largely, to restricted motion between forefoot and rearfoot. It is conceivable that, at faster gaits, a stiffer foot could enhance force transmission during midstance and enable the propulsive forces to be transmitted more promptly to the ground.
Conflict of interest The authors would like to state that no conflict of interest exists in relation to any part of the work.
Acknowledgement The authors gratefully acknowledge support from the Anatomical Society of Great Britain and Ireland. References Andriacchi, T.P., Ogle, J.A., Galante, J.O., 1977. Walking speed as a basis for normal and abnormal gait measurements. Journal of Biomechanics 10, 261–268. Benedetti, M.G., Leardini, A., Bianchi, L., Berti, L., Giannini, S., 2008. Comparison of outputs of different models for foot kinematics, The International Foot and Ankle Biomechanics Community, Istituto Ortopedico Rizzoli, Bologna, Italy. Caravaggi, P., Pataky, T., Goulermas, J.Y., Savage, R., Crompton, R., 2009. A dynamic model of the windlass mechanism of the foot: evidence for early stance phase preloading of the plantar aponeurosis. Journal of Experimental Biology 212, 2491–2499.
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Carson, M.C., Harrington, M.E., Thompson, N., O’Connor, J.J., Theologis, T.N., 2001. Kinematic analysis of a multi-segment foot model for research and clinical applications: a repeatability analysis. Journal of Biomechanics 34, 1299–1307. Cavanagh, P.R., Rodgers, M.M., 1985. Pressure distribution underneath the human foot. In: Schneider, S.M.P.E. (Ed.), Biomechanics: Current Interdisciplinary Research. Martinus Nijhoff, Dordrecht, The Netherlands, pp. 85–95. Clarke, T.E., 1980. The pressure distribution under the foot during barefoot walking. Unpublished Ph.D. Thesis. The Pennsylvania State University, University Park. D’Andrea, S., Tylkowski, C., Losito, J., Arguedas, W., Bushman, T., Howell, V., 1993. Three-dimensional kinematics of the foot. In: proceedings of the eighth Annual East Coast Clinical Gait Conference, Rochester, MN, USA, pp. 109–110. DeLozier, G., Alexander, I., Narayanaswamy, R., 1991. A method for measurement of integrated foot kinematics. In: proceedings of the International Symposium on Three-Dimensional Analysis of Human Movement, Montreal, Canada, pp. 79–82. Grood, E.S., Suntay, W.J., 1983. A joint coordinate system for the clinical description of three-dimensional motions: application to the knee. Journal of Biomechanical Engineering 105, 136–144. Hicks, J.H., 1954. The mechanics of the foot. II. The plantar aponeurosis and the arch. Journal of Anatomy 88, 25–30. Hof, A.L., Elzinga, H., Grimmius, W., Halbertsma, J.P., 2002. Speed dependence of averaged EMG profiles in walking. Gait Posture 16, 78–86. Hunt, A.E., Smith, R.M., Torode, M., Keenan, A.M., 2001. Inter-segment foot motion and ground reaction forces over the stance phase of walking. Clinical Biomechanics 16, 592–600. Kidder, S.M., Abuzzahab Jr., F.S., Harris, G.F., Johnson, J.E, 1996. A system for the analysis of foot and ankle kinematics during gait. IEEE Transactions on Rehabilitation Engineering 4, 25–32. Kirtley, C., Whittle, M.W., Jefferson, R.J., 1985. Influence of walking speed on gait parameters. Journal of Biomedical Engineering 7, 282–288. Leardini, A., Benedetti, M.G., Berti, L., Bettinelli, D., Nativo, R., Giannini, S., 2007. Rear-foot, mid-foot and fore-foot motion during the stance phase of gait. Gait Posture 25, 453–462. Leardini, A., Benedetti, M.G., Catani, F., Simoncini, L., Giannini, S., 1999. An anatomically based protocol for the description of foot segment kinematics during gait. Clinical Biomechanics (Bristol, Avon) 14, 528–536. Lundberg, A., Goldie, I., Kalin, B., Selvik, G., 1989a. Kinematics of the ankle/foot complex: plantarflexion and dorsiflexion. Foot Ankle 9, 194–200. Lundberg, A., Svensson, O.K., Bylund, C., Goldie, I., Selvik, G., 1989b. Kinematics of the ankle/foot complex—part 2: pronation and supination. Foot Ankle 9, 248–253.
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Lundberg, A., Svensson, O.K., Bylund, C., Selvik, G., 1989c. Kinematics of the ankle/ foot complex—part 3: influence of leg rotation. Foot Ankle 9, 304–309. Mann, H.B., Whitney, D.R., 1947. On a test of whether one of two random variables is stochastically larger than the other. The Annals of Mathematical Statistics 18, 50–60. Mann, R., Inman, V.T., 1964. Phasic activity of intrinsic muscles of the foot. The Journal of Bone and Joint Surgery 46, 469–481. Murray, M.P., Mollinger, L.A., Gardner, G.M., Sepic, S.B., 1984. Kinematic and EMG patterns during slow, free, and fast walking. Journal of Orthopaedic Research 2, 272–280. Neptune, R.R., Sasaki, K, 2005. Ankle plantar flexor force production is an important determinant of the preferred walk-to-run transition speed. Journal of Experimental Biology 208, 799–808. Nester, C., Jones, R.K., Liu, A., Howard, D., Lundberg, A., Arndt, A., Lundgren, P., Stacoff, A., Wolf, P., 2007. Foot kinematics during walking measured using bone and surface mounted markers. Journal of Biomechanics 40, 3412–3423. Nilsson, J., Thorstensson, A., 1989. Ground reaction forces at different speeds of human walking and running. Acta Physiologica Scandinavica 136, 217–227. Pataky, T.C., Caravaggi, P., Savage, R., Parker, D., Goulermas, J.Y., Sellers, W.I., Crompton, R.H., 2008. New insights into the plantar pressure correlates of walking speed using pedobarographic statistical parametric mapping (pSPM). Journal of Biomechanics 41, 1987–1994. Rattanaprasert, U., Smith, R., Sullivan, M., Gilleard, W., 1999. Three-dimensional kinematics of the forefoot, rearfoot, and leg without the function of tibialis posterior in comparison with normals during stance phase of walking. Clinical Biomechanics 14, 14–23. Rosenbaum, D., Hautmann, S., Gold, M., Claes, L., 1994. Effects of walking speed on plantar pressure patterns and hindfoot angular motion. Gait & Posture 2, 191–197. Scott, S.H., Winter, D.A., 1991. Talocrural and talocalcaneal joint kinematics and kinetics during the stance phase of walking. Journal of Biomechanics 24, 743–752. Tulchin, K., Orendurff, M.S., Adolfsen, S., Karol, L., 2009. The effects of walking speed on multisegment foot kinematics in adults. Journal of Applied Biomechanics 25, 377–386. Wu, G., Siegler, S., Allard, P., Kirtley, C., Leardini, A., Rosenbaum, D., Whittle, M., D’Lima, D.D., Cristofolini, L., Witte, H., Schmid, O., Stokes, I., 2002. ISB recommendation on definitions of joint coordinate system of various joints for the reporting of human joint motion—part I: ankle, hip, and spine. International Society of Biomechanics. Journal of Biomechanics 35, 543–548.
Contents lists available at ScienceDirect
Journal of Biomechanics journal homepage: www.elsevier.com/locate/jbiomech www.JBiomech.com
Kinematic correlates of walking cadence in the foot Paolo Caravaggi a,n, Alberto Leardini b,1, Robin Crompton a,2 a b
HACB, School of Biomedical Sciences, University of Liverpool, Sherrington Buildings, Liverpool L69 3GE, UK Movement Analysis Laboratory, Istituto Ortopedico Rizzoli, Bologna, Italy
a r t i c l e in fo
abstract
Article history: Accepted 9 April 2010
Evidence has frequently been reported of modifications in gait patterns within the lower limb related to the cadence of walking. Most reports have concerned relationships between cadence and kinematic and the kinetic changes occurring in the main joints and muscles of the lower limb as a whole. The aim of the present study was to assess whether significant changes are also measurable in kinematics of the foot segments. An existing 15 marker-set protocol allowed a four-segment foot and shank model to be defined for relative rotations between the segments to be calculated. Stereophotogrammetry was employed to record marker position data from ten subjects walking at three cadences. The slow- and normal cadence datasets showed similar profiles of joint rotation in three anatomical planes, but significant differences were found between these and the fast cadence. At all joints, frame-by-frame statistical analysis revealed increased dorsiflexion from heel-strike to midstance (po 0.05) and increased plantarflexion from midstance to toe-off (po 0.05) with increasing cadence. From foot-flat to heel-rise, the fast cadence kinematic data showed a decreased range of motion in the sagittal-plane between forefoot and rearfoot (3.21 7 1.21 at slow cadence; 2.01 7 0.81 at fast cadence; p o 0.05). The cadences imposed and the multisegment protocol revealed significant kinematic changes in the joints of the foot during barefoot walking. & 2010 Elsevier Ltd. All rights reserved.
Keywords: Multisegment foot kinematics Joints of the foot Motion analysis
1. Introduction Over the last decade it has become apparent that reduction of the foot to a single segment oversimplifies its role in lower limb dynamics during gait. The pioneering work of Lundberg et al. (1989a,b,c), using roentgenographic analysis, stimulated interest in the investigation of motion occurring at the internal joints of the foot (DeLozier et al., 1991; Scott and Winter, 1991; D’Andrea et al., 1993). The outcome of these studies and advances in stereophotogrammetric technique have motivated researchers to design non-invasive surface marker protocols to measure internal joint motion in the foot, for clinical and general biomechanical investigations, in order to provide a more detailed description of the foot’s complex kinematics. Two- (Rattanaprasert et al., 1999; Hunt et al., 2001), three- (Kidder et al., 1996; Carson et al., 2001) and four-segment (Leardini et al., 1999; Leardini et al., 2007) three-dimensional rigid-body models of the foot have been proposed. These have indeed revealed that skin-mounted markers can consistently, and with a good degree of repeatability, detect significant amounts of motion at the major joints in all three
n
Corresponding author. Tel.: + 44 151 794 6867; fax: + 44 151 794 5517. E-mail addresses: [email protected] (P. Caravaggi), [email protected] (A. Leardini), [email protected] (R. Crompton). 1 Tel.: + 39 051 6366522; fax: + 39 051 6366561. 2 Tel.: + 44 151 794 5456; fax: +44 151 794 5517. 0021-9290/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jbiomech.2010.04.015
anatomical planes. Moreover, mean differences between joint rotation data derived from tracking bone-pins and skin markers have been reported to be greater than 31 in only 35% of the kinematic data during stance (Nester et al., 2007). However, a lack of standardization in the definition of neutral angles between the segments, in the bony landmarks employed, in the definition of local reference frames and scarcity and/or non-uniformity of published data make comparison of the results from different studies difficult. An attempt to compare the ranges of motion and the temporal profiles of rotation angles between different multisegment foot models (Benedetti et al., 2008) concluded that only rotations in the sagittal-plane at the rearfoot and at the first metatarsophalangeal joint were consistently reproduced by different methodologies. Although walking speed has been shown to affect the kinematics and kinetics in the lower limbs (Murray et al., 1984; Kirtley et al., 1985), if, and where, any walking-speed-related modifications also occur in the foot has not been fully addressed. The inference that significant kinematic changes must occur along the longitudinal arch of the foot when walking at faster gaits finds support in early pedobarographic studies (Clarke, 1980; Cavanagh and Rodgers, 1985; Rosenbaum et al., 1994), and more recently in an application of a novel technique to assess differences in pressure records (Pataky et al., 2008), which revealed that midfoot and proximal forefoot peak plantar pressures are negatively correlated with walking speed. To the best of the authors’ knowledge, only
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one study has tried to assess the influence of walking speed on foot kinematics (Tulchin et al., 2009). In that study, however, the marker protocol employed did not allow for any tracking of the midfoot and only sagittal-plane rotations were reported. Therefore, for the present study, a more complete foot protocol (Leardini et al., 2007) was chosen, based on a clear definition of the bony landmarks and of the local reference frames and designed to meet the recommendations of the International Society of Biomechanics (Wu et al., 2002).
From a clinical perspective, a study of the influence of walking speed on foot kinematics would allow clinicians to take account of possible speed-related kinematic modifications when employing multisegment models to assess the alterations occurring at the main joints of the foot pre- and post-operatively, or to evaluate the overall effects of treatments. In fact progression speed frequently cannot be controlled in clinical gait analysis, and therefore the possibility of influence by established speed-related biases should be considered during clinical interpretation. Consequently, the main goal of this investigation was to test if significant kinematic changes do occur between foot segments when walking at different speeds. For this purpose, we adopted the skin-mounted marker protocol devised by Leardini et al. (2007), which allows tracking of the six degrees-of-freedom motion of the shank, calcaneus, midfoot and metatarsal segments.
2. Methods
Fig. 1. The reflective markers attached to the lower limb and foot of one of the subjects who volunteered in the study.
A six-camera motion capture system set to 250 Hz (ProReflex 1000 MCU, Qualysis, Gothenburg, Sweden) was employed to collect marker trajectories for the foot segment kinematics analysis. Ten healthy young male subjects (age 29.37 6.4 yrs; height 178.8 76.0 cm and weight 73.8 78.7 Kg) with no history of lower limb main injuries nor gross musculoskeletal abnormalities of the lower limb (two subjects had relatively low-arched feet) were analysed during walking on a 6 m long wooden walkway. Simultaneously, a Kistler force platform (model 9281C, Kistler Instruments Ltd., Hook, Hampshire, UK) recorded ground reaction force (GRF) at 500 Hz. The left shank and foot of each subject were instrumented with fifteen 7 mm diameter reflective markers, attached to the skin with doublesided adhesive tape (Fig. 1), according to Leardini et al. (2007). Before starting the walking trials, in order to define the neutral position of the foot, a 1 s static acquisition was taken with the subject standing still in a right-leg support (Caravaggi et al., 2009), the left foot in contact with the floor but with minimum load, i.e. no-weight bearing for the analysed leg. Each subject was then asked to walk at three subjectively determined cadences: normal, slow and fast. Slow and fast speeds were described to the subjects as the slowest and the fastest natural gaits that they could reproducibly achieve. In order to minimize intra-subject speed variability, and before starting data acquisition, each subject was requested to practice the different gait speeds until he felt comfortable in reproducing each walking speed. Ten walking trials were recorded for each subject at each of the three cadences. Triplanar intersegment rotations for the shank/calcaneus, calcaneus/midfoot, midfoot/metatarsus and calcaneus/metatarsus joints were calculated (Grood and Suntay, 1983; Leardini et al., 2007) to derive dorsiflexion/plantarflexion, eversion/inversion and abduction/adduction, respectively in the sagittal, frontal and transverse planes. Frame-by-frame statistical differences between time-histories of the rotations in each sample within the normalized stance phase duration and between the relevant ranges of
1.2 1.1
Stance duration [s]
1 0.9 0.8 0.7 0.6 0.5 0.4
slow
normal
fast
Cadence group Fig. 2. Stance phase durations across 100 trials per walking cadence group (slow, normal and fast).
P. Caravaggi et al. / Journal of Biomechanics 43 (2010) 2425–2433
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duration across the 100 trials per cadence group are plotted for each trial/subject/cadence combination in Fig. 2. Inter-subject means (7standard deviation) of stance phase duration were 0.834 s ( 70.097 s), 0.652 s (70.068 s) and 0.533 s ( 70.046 s), respectively for the slow, normal and fast cadences. The estimated inter-subject means (7standard deviations) of cadence (steps/min) were 88.1 ( 710.3), 110.1 ( 711.3) and 130.2 ( 711.0), respectively for the slow, normal and fast cadence sets. A clear trend of longer stance duration for slower cadence can be detected, though associated also with larger inter-subject variability. In agreement with previous findings (Andriacchi et al., 1977; Nilsson and Thorstensson, 1989), analysis of the GRF revealed that increasing cadence was accompanied by higher peaks within the time-histories of the three GRF components (Fig. 3). This was especially true for the first two peaks of the vertical component, i.e. in early- (1.0270.07BW in slow walking; 1.4070.13BW in fast walking: p o0.001) and mid-stance (0.85 70.05BW in slow walking; 0.4970.01BW in fast walking: po0.001), and for the two peaks of the anterior–posterior component in early(0.1470.03BW in slow walking; 0.2970.06BW in fast walking: po0.001) and late-stance (0.17 70.02BW in slow walking; 0.2570.05BW in fast walking: p o0.001). Slow- and normal cadence sets displayed similar rotation profiles, but differences, however, existed between these two groups on the one hand and fast walking on the other hand (Fig. 4). Kinematic data from the normal walking group are largely in agreement with the report of Leardini et al. (2007), the only evident difference being in sagittal-plane rotation between calcaneus and midfoot (Fig. 5, top). The inter-trial variability, averaged over stance duration, of joint rotations for 10 repetitions from the same subject, and for one walking cadence, was between 70.31 and 71.01, the sagittal-plane rotation between shank and calcaneus showing the largest variability, most likely because of the correspondingly large range. Frame-by-frame statistical analyses performed separately for each sample of the rotation time-histories in the three anatomical planes from slow- and fastcadence groups are shown in Fig. 6, and are commented upon individually in the following subsections. Where not explicitly reported, the results presented below should be considered to be statistically significant at 95% confidence level.
3.1. Effect of cadence on sagittal-plane motion
Fig. 3. Inter-subject mean temporal profiles of ground reaction forces across 10 subjects and 100 trials at three walking cadences. From top to bottom: vertical GRF; anterior–posterior GRF and medio-lateral GRF. Positive GRF are directed upwards, anteriorly and medially, respectively. motion (ROM) for different walking speeds were tested using the non-parametric Mann–Whitney U-test (Mann and Whitney, 1947). From the measured stance duration, cadence was estimated according to the values of the gait cycle durations calculated from the correlation between the stance interval as percentage of the gait cycle and the walking speed (Kirtley et al. (1985). Average walking speed associated with the three cadences was taken from a previous work (Pataky et al., 2008).
3. Results Three (slow, normal and fast) different, and consistent, mean patterns of walking were obtained. The values of stance phase
For all joints, increased cadence appeared to modify the pattern of rotation in the sagittal-plane in two contrasting ways at different stance phases: by increasing dorsiflexion from around heel-strike to midstance; and by increasing plantarflexion from around midstance to toe-off (Fig. 6). The midtarsal joint was more dorsiflexed from around 5% to 40% of stance and more plantarflexed from around 60% to 100% of stance when comparing the fast- to the slow cadence sets.
3.2. Effect of cadence on frontal plane motion With increase in the cadence, the calcaneus was found to be more inverted with respect to the shank from around midstance to push-off (around 80% of stance); but more everted just before toe-off (Fig. 6). Similarly, the midfoot segment was more inverted with reference to the calcaneus from midstance to push-off. The metatarsus was more inverted with reference to the calcaneus up to midstance; but more everted during late stance, albeit for a shorter period.
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Fig. 4. Left to right: mean temporal profiles of the rotation angles between: shank and calcaneus; calcaneus and midfoot; midfoot and metatarsus and calcaneus and metatarsus across 10 subjects and 100 trials at three walking cadences during normalized stance phase. From top to bottom: dorsiflexion/plantarflexion; eversion/inversion and abduction/adduction.
Fig. 5. Mean temporal profiles (7 1 SD) of the three rotation angles between calcaneus and midfoot across 10 subjects and 100 trials at normal cadence during normalized stance phase. From top to bottom: dorsiflexion/plantarflexion; eversion/inversion and abduction/adduction.
3.3. Effect of cadence on transverse plane motion The calcaneus was more adducted with reference to the shank during late stance. The midfoot was more abducted with reference to the calcaneus up to midstance; but more adducted around push-off, albeit for a shorter period (Fig. 6). During two relatively short phases, just prior to and just after midstance, the metatarsus was, respectively, more adducted and more abducted with reference to the midfoot. The metatarsus was more adducted with reference to the calcaneus from around midstance to pushoff.
3.4. Analysis of the range of motion Analysis of the triplanar joint ROM confirmed the inference from visual inspection of the mean temporal profiles of the
2429 Fig. 6. In black, time-normalized intervals of those rotation angles statistically different between slow and fast walking cadences at 95% confidence interval. From top to bottom: comparison of joint rotations in the sagittal, frontal and transverse planes. From left to right, between: shank and calcaneus; calcaneus and midfoot; midfoot and metatarsus and calcaneus and metatarsus. (e.g. for sagittal-plane rotations) Positive (+1) ranges designate greater dorsiflexion at fast cadence; negative ( 1) ranges designate greater plantarflexion at fast cadence and zero ranges designate sagittal-plane rotation angles not statistically different between slow and fast cadences.
P. Caravaggi et al. / Journal of Biomechanics 43 (2010) 2425–2433
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Table 1 Triplanar range of motion values [deg] between shank and calcaneus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
6.7 3.6 1.1 3.5 1.0 0.8 11.5 2.9 3.0 6.4 1.9 2.1 11.6 2.1 2.7 21.6 6.2 6.1 5.2 1.2 1.7
6.9 3.3 0.9 3.6 0.8 0.6 10.8 2.6 2.4 6.6 2.1 1.9 11.4 2.1 2.2 22.1 5.9 5.4 5.3 1.0 1.5
1.8 1.4 0.7 1.2 0.8 0.6 3.7 1.1 1.9 2.6 1.0 1.4 4.0 0.9 1.7 6.6 1.9 3.4 1.9 0.7 0.9
6.7 4.2 1.2 4.1 0.9 0.8 9.8 2.9 2.8 7.1 1.9 2.2 11.1 2.5 2.7 22.2 6.3 6.3 6.2 1.4 1.8
6.7 4.1 1.1 4.0 0.6 0.6 8.8 2.7 2.0 6.9 1.7 1.9 10.9 2.4 2.2 21.9 5.9 6.2 6.0 1.3 1.4
1.6 1.7 0.7 1.1 0.8 0.5 3.9 1.2 1.8 2.9 0.9 1.4 3.5 1.3 1.5 7.0 1.8 3.5 2.4 0.8 1.1
6.7 4.3 1.4 4.9 0.9 0.8 7.5 2.8 2.9 7.6 1.5 2.2 8.5 2.3 2.0 22.8 6.2 6.4 6.4 1.6 1.8
6.7 4.3 1.0 5.1 0.5 0.6 7.2 2.7 2.4 7.2 1.3 1.8 7.8 2.2 1.9 22.4 5.8 5.9 6.1 1.5 1.3
2.1 2.0 1.1 1.6 1.0 0.5 2.9 1.2 1.8 2.4 0.9 1.5 2.8 1.6 1.2 5.8 1.7 3.6 2.4 0.9 1.5
p1
p2
n
n
n
n n
n
n
n
n
n n
n
n
n
n
n
n n
p3
n n
Table 2 Triplanar range of motion values [deg] between calcaneus and midfoot during seven phases of stance and for three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
p1
p2
p3
1.5 1.7 1.3 0.9 1.8 0.7 7.1 3.1 1.9 3.9 2.2 2.0 5.6 1.6 2.0 10.9 7.1 5.4 2.9 1.4 1.1
1.4 1.4 0.9 0.7 1.7 0.7 6.9 3.1 1.7 3.7 1.9 1.7 5.1 1.3 1.6 11.0 7.0 5.1 3.0 1.2 1.0
0.9 1.2 1.0 0.6 0.8 0.5 1.4 1.0 0.8 1.6 1.2 1.3 2.3 1.1 1.4 1.7 1.9 1.9 1.0 0.7 0.5
1.8 1.9 1.3 1.0 1.9 0.9 6.5 3.0 1.9 4.2 2.3 2.3 5.2 1.6 1.9 11.0 6.8 5.6 2.8 1.1 1.1
1.7 1.7 1.1 0.9 1.8 0.9 6.1 3.0 1.8 3.9 2.1 1.9 4.6 1.5 1.5 11.1 6.9 4.9 2.7 1.1 1.0
1.1 1.1 1.3 0.6 0.8 0.5 1.5 1.1 0.9 1.9 1.1 1.4 2.6 1.0 1.5 2.1 1.9 2.2 1.1 0.5 0.6
2.1 2.1 1.5 1.0 2.1 1.1 5.1 3.3 2.2 4.7 1.6 2.6 4.6 1.7 2.1 10.8 6.6 6.2 2.2 1.2 0.9
2.0 1.8 1.2 1.0 2.0 0.9 4.5 2.8 1.8 4.5 1.7 2.7 3.6 1.1 1.9 10.9 6.7 5.7 2.2 1.1 0.8
1.2 1.3 1.2 0.6 1.1 0.6 1.8 1.5 1.1 1.7 0.8 1.3 3.1 1.3 1.4 2.4 1.8 2.1 1.0 0.6 0.5
n
n n
n
rotation angles, that it was only the slow versus fast cadence comparison which displayed the evident variation (Tables 1–4). All foot joints showed increased ROM in the sagittal-plane during early stance with increasing cadence. With the exception of the midfoot/metatarsus joint, the total sagittal-plane ROM during normalized stance phase duration was unaffected by walking cadence. Analysis of the ROM in the interval between 21% and 80% of normalized stance revealed a decrease in both the
n
n n n
n
n
n n n n
n
n n
n n
n n
n
n
relative sagittal-plane ROM between calcaneus and midfoot (7.1171.41 at slow cadence; 5.1171.81 at fast cadence: po0.001) and of relative sagittal-plane ROM between calcaneus and metatarsus (5.61 71.31 at slow cadence; 4.6171.61 at fast cadence: p o0.001). In contrast, during the same interval, the sagittal-plane ROM between midfoot and metatarsus increased from 3.6171.01 at slow cadence to 5.9171.81 at fast cadence (p o0.001). In the interval foot-flat to heel-rise (which covers the
P. Caravaggi et al. / Journal of Biomechanics 43 (2010) 2425–2433
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Table 3 Triplanar range of motion values [deg] between midfoot and metatarsus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
1.1 1.4 1.1 0.9 2.4 0.7 3.6 2.9 2.8 4.0 1.1 1.2 2.3 2.0 2.0 10.4 5.2 5.3 1.1 0.7 1.3
1.0 1.2 0.9 0.7 2.1 0.6 3.5 2.9 2.2 4.2 0.9 1.3 2.0 1.7 1.8 10.9 4.7 5.3 0.9 0.6 1.1
0.8 0.8 0.7 0.6 1.3 0.5 1.0 0.9 1.6 1.5 0.8 0.6 1.5 1.3 1.3 2.8 2.0 1.7 0.9 0.4 0.7
1.4 1.6 1.1 1.0 2.5 0.9 4.3 3.0 2.8 4.3 1.0 1.2 2.4 1.8 2.3 11.3 5.1 5.6 1.0 0.8 1.1
1.0 1.5 1.0 0.8 2.2 1.0 4.2 3.0 2.3 4.4 0.9 1.2 2.1 1.4 2.1 11.9 4.6 5.7 0.8 0.6 1.0
1.0 1.0 0.9 0.7 1.2 0.5 1.2 0.8 1.7 1.3 0.6 0.6 1.6 1.5 1.4 2.9 1.9 1.7 0.7 0.5 0.6
1.5 1.5 1.2 1.1 2.5 0.9 5.9 3.2 2.7 4.0 0.9 0.9 3.1 1.7 2.6 12.4 5.2 5.6 1.0 1.0 0.9
1.2 1.3 0.9 0.8 2.3 0.8 5.8 3.0 2.3 3.8 0.8 0.9 2.2 0.9 2.1 13.3 4.9 5.5 0.9 0.8 0.8
1.0 0.9 0.9 0.8 1.3 0.5 1.8 1.0 1.7 1.4 0.4 0.6 3.0 1.6 2.1 3.5 2.0 1.9 0.6 0.6 0.5
p1
p2
p3
n
n n n
n
n
n
n
n
n
n
n
n
n n
n n
Table 4 Triplanar range of motion values [deg] between calcaneus and metatarsus during seven phases of stance and for the three walking cadence groups. Where DP, EI and AA are rotations in the sagittal, frontal and transverse planes, respectively. Means, medians and SD of the ROM values have been computed across 100 walking trials for each walking cadence group. The asterisks indicate inter-cadence comparisons statistically different at 95% confidence interval where: p1 is the comparison Slow vs. Normal walking group; p2 is the comparison Slow vs. Fast walking group, and p3 is the comparison Normal vs. Fast walking group. Phase
0–10%
11–20%
21–80%
81–90%
91–100%
0–100%
foot-flat to heel-rise
Rotation
DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA DP EI AA
Slow
Normal
Fast
Statistical significant difference
Mean
Median
SD
Mean
Median
SD
Mean
Median
SD
p1
p2
1.7 1.6 2.1 1.3 2.3 1.3 5.6 3.2 4.0 7.9 2.0 3.0 6.1 3.3 2.4 17.6 7.1 8.2 3.2 1.0 1.1
1.5 1.4 1.5 1.1 2.1 1.1 5.4 3.3 3.9 7.8 2.0 2.9 5.4 2.8 2.2 17.9 6.3 8.0 3.2 0.8 1.1
0.9 0.7 1.5 0.9 1.2 0.8 1.3 1.0 1.6 2.1 1.0 1.6 3.4 2.2 1.2 2.8 2.8 2.4 1.2 0.6 0.6
2.2 1.6 2.2 1.4 2.3 1.2 4.8 3.0 4.4 8.5 2.4 3.2 5.7 3.3 2.9 18.1 7.2 8.6 2.9 1.1 1.1
1.9 1.6 2.1 1.3 2.2 1.3 4.8 2.9 4.1 8.1 2.3 2.9 5.2 2.3 2.5 18.2 6.6 8.9 3.0 0.9 1.0
1.1 0.8 1.3 1.0 1.2 0.6 1.1 0.9 1.9 2.1 1.2 1.7 3.0 2.4 1.5 2.6 2.8 2.9 0.9 0.7 0.6
2.5 1.8 2.1 1.5 2.3 1.6 4.6 2.6 4.9 8.5 3.0 2.2 4.4 3.1 2.9 18.0 8.1 7.9 2.0 1.2 1.1
2.0 1.6 2.0 1.2 2.2 1.6 4.5 2.6 4.5 8.3 3.3 2.2 3.4 2.5 3.0 17.8 7.4 7.5 2.0 1.1 0.9
1.3 1.2 1.2 1.2 1.2 0.9 1.6 0.9 2.3 1.8 1.4 1.3 2.8 2.3 1.8 3.4 3.1 2.9 0.8 0.6 0.7
n
n
part of the stance phase during which the whole sole of the foot is in contact with the ground), the sagittal-plane ROM between foot joints was either unaffected by, or decreased with cadence.
4. Discussion Prior to this study, because of the small degree of motion at the joints of the foot, and due to the limited techniques utilised, it had not yet been fully established whether significant kinematic
n
n
n
n n n n n n n n
p3
n n
n n n
n n
n
n n
n
changes occur at the foot joints between different walking cadences. A carefully configured stereophotogrammetric system with six cameras and a recently established multisegment protocol with 15 markers were exploited over ten normal subjects to identify the possible alterations in ground reaction force and in the rotations at four main foot joints during the stance phase of barefoot walking at three self-determined cadences. Frame-byframe statistical analysis revealed interesting differences. Analysis of the mean kinematics profiles (Fig. 4) and of the ROM (Tables 1 to 4) revealed that most joint motion occurred in
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the sagittal-plane but cadence appeared to significantly affect rotations in all three anatomical planes. The continuity and lengths of the time-normalized intervals (Fig. 6) indicate that increase in the cadence systematically affects joint kinematics in the foot. The pattern of cadence-dependent joint kinematic changes in the sagittal-plane was clearly distinct in early and late phases: increased segment dorsiflexion up to around midstance, but increased segment plantarflexion from midstance to toe-off (Fig. 6, top plots). In the frontal plane, in general, increased cadence seemed correlated with greater inversion between foot segments (Fig. 6, middle plots).The statistical analysis showed that both the midtarsal joint, between calcaneus and midfoot, and the tarsometatarsal joint, between midfoot and metatarsus, appeared to be involved in absorbing the vertical forces arising during early stance (Fig. 4 and Fig. 6, from around 5% to 40% for the midtarsal joint). This appears to be a consequence of the higher vertical impact on the foot in early stance with increasing walking speed (Fig. 3, top plot), which acts to increase joint dorsiflexion. However, in accordance with the sequence of kinematic events at the rearfoot, the tarsometatarsal joint appears to contribute to absorbing the vertical component of the GRF only later, from around 20% of the stance (during foot-flat). While the tarsometatarsal joint maintained a slightly dorsiflexed position until heel-rise, the midfoot continued dorsiflexing until push-off (around 80% of stance). Higher mobility of the midtarsal joint in the sagittal-plane finds confirmation in the analysis of its ROM in the interval 21%–80% of stance, which for the normal cadence set, for example, showed a total value of 6.5171.51 (Table 2) and for the metatarsus relative to the midfoot of 4.3171.21 (Table 3). Our kinematic data are in agreement with Tulchin et al. (2009) in showing that hindfoot and forefoot display a clear shift towards plantarflexion with increasing walking cadence. However, the detailed frame-by-frame statistical analysis of the present investigation allows clear identification of when, and where, these cadence-dependent kinematic changes occur. Moreover, some major kinematic changes were also recorded in the frontal and the transverse planes, despite their limited motion and despite the fact that the skin motion errors, which intrinsically affect these measurements, might have been expected to have prevented identification of patterns as clear as those which were observed in the sagittal-plane. A further addition to the finding of Tulchin et al. (2009) is that the chosen marker-set allowed for a midfoot segment to be analysed, which permitted estimation of the individual contributions of midtarsal and tarsometatarsal joints to longitudinal arch deformation. Analysis of the joint ROM in the interval foot-flat to heel-rise revealed either decreased or unaffected sagittal-plane motion between foot segments with increasing walking cadence. Decreased vertical GRF at higher cadences in the central part of stance (Fig. 3) could certainly contribute to apparent archstiffening but cannot alone provide an explanation for increased plantarflexion from midstance until toe-off (Fig. 6). It therefore seems sensible to consider a possible active contribution to archaugmentation from the intrinsic muscles of the foot. The timing of activity onset of the intrinsic muscles, which work in synergy, as a functional unit, to support the medial longitudinal arch (Mann and Inman, 1964), appears well correlated with the pattern of plantarflexion identified in this investigation. Therefore, the combined action of the windlass mechanism (Hicks, 1954) and of the arch-supporting intrinsic and extrinsic muscles, such as the tibialis posterior, the activities of which are likely to increase with increasing walking speed (Hof et al., 2002; Neptune and Sasaki, 2005), can not only act to restrain segment dorsiflexion at midstance but also to increase the segment plantarflexion in late stance. The present detailed kinematic analysis of the foot joints supports the inference of some manner of arch-stiffening
mechanism at increasing walking cadence, as recently highlighted by pedobarographic analysis (Pataky et al., 2008). Most of the mean temporal profiles of the rotation angles for the normal walking group (Fig. 4) proved similar to those reported by Leardini et al. (2007). The most evident differences were in the larger sagittal-plane motion found between the calcaneus and midfoot segments and in the less pronounced eversion found between the midfoot and metatarsus during late stance in the present study. In contrast to Leardini et al. (2007), this study revealed a clear pattern of dorsiflexion between calcaneus and midfoot lasting until late stance, and subsequent plantarflexion at toe-off (Fig. 5, top), a pattern of motion more in agreement with the findings of Nester et al. (2007) who reported temporal profiles of sagittal-plane rotation, between calcaneus and navicular, and between calcaneus and cuboid, very similar to that between calcaneus and midfoot in the present study. Further, the total ROM of 8.6173.11 between those joints reported by Nester et al. (2007), was only slightly lower than that measured in this study (10.91 71.71, see Table 2). The discrepancies highlighted above could be the consequence of differences in the populations and/or the results of the sensitivity of the protocol to minor differences/ errors in the localization of the bony landmarks and relevant marker attachment. An existing foot and shank gait analysis protocol enabled careful assessment of the kinematic changes occurring in the joints of the foot when walking at three different cadences. These consistently affected rotations at the ankle, midtarsal and tarsometatarsal joints; i.e. increased cadence resulted in increased dorsiflexion in early stance and increased plantarflexion in late stance, accompanied also by a general increase in inversion. Since walking cadence has significant effects on foot kinematics, a direct implication of this study for clinical practice is that, whenever possible, walking cadence should be controlled and reported together with kinematic data. It is essential that kinematic variations due to foot pathologies or following surgery can be properly assessed in relation to the altered walking speed of the subject. Finally, the detailed analysis of the ROM revealed that, during midstance, increased cadence is related to restricted sagittalplane motion at the midtarsal joint and, more largely, to restricted motion between forefoot and rearfoot. It is conceivable that, at faster gaits, a stiffer foot could enhance force transmission during midstance and enable the propulsive forces to be transmitted more promptly to the ground.
Conflict of interest The authors would like to state that no conflict of interest exists in relation to any part of the work.
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