JCLB-03776; No of Pages 6 Clinical Biomechanics xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Gait adaptation during walking on an inclined pathway following spinal cord injury Emilie Desrosiers a,⁎, Cyril Duclos a,b, Sylvie Nadeau a,b a b
School of rehabilitation, Faculty of medicine, Universite de Montreal, Montreal, Canada Laboratoire de pathokinesiologie, Centre de recherche interdisciplinaire en readaptation (CRIR), Institut de readaptation Gingras-Lindsay-de-Montreal, Montreal, Quebec, Canada
a r t i c l e
i n f o
Article history: Received 2 December 2013 Accepted 8 April 2014 Keywords: Gait adaptation Inclined pathway Biomechanics Spinal cord injury Rehabilitation
a b s t r a c t Background: Individuals with incomplete spinal cord injury need to be assessed in different environments. The objective of this study was to compare lower-limb power generation in subjects with spinal cord injury and healthy subjects while walking on an inclined pathway. Methods: Eleven subjects with spinal cord injury and eleven healthy subjects walked on an inclined pathway at their natural gait speed and at slow gait speed (healthy subjects only). Ground reaction forces were recorded by force plates embedded in the inclined pathway and a 3-D motion analysis system recorded lower-limb motions. Data analysis included gait cycle parameters and joint peak powers. Differences were identified by student t-tests. Findings: Gait cycle parameters were lower in spinal cord injury subjects compared to healthy subjects at natural speed but similar at slow gait speed. Subjects with spinal cord injury presented lower power at the ankle, knee and hip compared to healthy subjects at natural gait speed while only the power generation at push-off remained lower when the two groups performed at similar speed. Interpretation: The most important differences are associated with the fact that individuals with spinal cord injury walk at a slower speed, except for the ankle power generation. This study demonstrated that, even with a good motor recovery, distal deficits remain and may limit the ability to adapt to uphill and downhill walking. Inclined pathways are indicated to train patients with spinal cord injury. Clinicians should focus on the speed of uphill and downhill walking and on the use of plantar flexors. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Recent medical progress has allowed an increase in the survival and functional independence of people following a spinal cord injury (SCI) (Whiteneck et al., 1992). Recovering independent walk is one of the main goals of individuals with SCI, especially in people with an incomplete lesion (Scivoletto and Di Donna, 2009). About 80 to 100% of AIS D individuals will recover the ability to walk one year post injury (Lemay and Nadeau, 2010). A person is classified as AIS D if the majority of muscles below the lesion have a motor score ≥3/5 according to the American Spinal Injury Association (ASIA) Scale (Scivoletto and Di Donna, 2009). A score ≥ 3/5 indicates that the muscle has the capacity to counteract gravity. The cause and severity of the SCI will have a major influence on the rehabilitation and the capacity to walk (Noonan et al., 2012). Despite a functional recovery of walk, many limitations such as a decrease in gait speed and endurance may remain following rehabilitation (Kim et al., 2004).
⁎ Corresponding author at: Laboratoire de pathokinesiologie, Centre de recherche interdisciplinaire en readaptation du Montreal metropolitain, Institut de readaptation Gingras-Lindsay-de-Montreal, 6300 Avenue Darlington, Montreal, Quebec H3S 2J4, Canada. E-mail address: [email protected] (E. Desrosiers).
Walking is a complex task that requires sufficient muscle strength, balance and coordination (Barbeau et al., 2006). For people with SCI, the strength of the leg muscles, particularly knee extensors and hip muscles, seems to be one of the principal factors that can predict their capacity to recover a functional walk (Barbeau et al., 2006; Kim et al., 2004). Meanwhile, other clinical factors such as spasticity, posture, cocontractions and loss of proprioception can limit the ability to walk (Barbeau et al., 2006; Brotherton et al., 2007; Leroux et al., 1999; Scivoletto et al., 2008). In addition to a decrease in step length and an increase in double time support in comparison to healthy individuals (Barbeau et al., 2006), subjects with SCI who are able to walk also present an increased knee flexion and an abnormal knee–hip coordination compared to healthy subjects (Leroux et al., 1999). Changes in muscular activation may limit their capacity to adapt their gait in different environments (Leroux et al., 1999). Moreover, the use of walking aids is frequent in this population to assist with negotiation of the environment. However, it also may increase energy expenditure and alter posture (Leroux et al., 2006). Walking on an inclined pathway requires changes in motor strategies to adapt to the ramp (Lay et al., 2006). During uphill walking, healthy subjects reduce their cadence (Prentice et al., 2004) and increase their step length (Kawamura et al., 1991; Leroux et al., 2002). There is also an increase in knee flexion at heel strike and an increased
http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004 0268-0033/© 2014 Elsevier Ltd. All rights reserved.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
2
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
leg extension during the stance phase (Lay et al., 2006) along with an increase in propulsion (Lay et al., 2006; Leroux et al., 2002) and in hip extensor and plantar flexor moments (Lay et al., 2007). During downhill walking, healthy subjects decrease their step length (Kuster et al., 1995; Leroux et al., 2002) and increase their cadence (Kawamura et al., 1991; Kuster et al., 1995; Lay et al., 2006). Healthy subjects also show an increase in their knee flexion during the stance phase (Lay et al., 2006; Leroux et al., 2002), knee extensors and dorsiflexor activity (Kuster et al., 1995; Lay et al., 2007) and breaking force (Lay et al., 2006, 2007). Few studies have quantified the adaptation of subjects with SCI walking on an inclined pathway. Their capacity to adapt to inclined surfaces seems to be correlated with their gait speed during level walking (Leroux et al., 1999, 2006). During uphill walking, subjects with SCI present an increase in hip and trunk flexion and a weak push-off at the end of the stance phase (Leroux et al., 1999). This constant trunk flexion position minimizes the gravity effect on the knee extensors during uphill walking but might reduce the capacity to adapt to downhill walking (Leroux et al., 2006). In fact, a normal adaptation is to present a backward tilt of the trunk as the descending slope increases (Leroux et al., 2002). With regard to these results, this population seems to present impaired adaptations to inclined walking which can lead to a loss of balance and an inefficient gait pattern characterized by a decreased walking speed. Authors agree that more studies are necessary to increase our understanding of the walking adaptation of people with SCI in more challenging environments to optimize their rehabilitation. Jayaraman et al. (2006) demonstrated that individuals with incomplete SCI presented deficits in generating peak isometric torque in the knee extensor and plantar flexor muscle groups during a voluntary contraction. Considering the role of the ankle in propulsion during walking, the difficulty in generating an adequate push-off could have a functional impact on their gait abilities. In addition, individuals with SCI generally present a decrease in angular excursion, reducing their capacity to produce high angular velocities and, consequently, decreasing lower-limb power values (Barbeau et al., 2006). Thus, because of the changes in kinetics and the frequent occurrence of uphill and downhill walking in daily living, it is necessary to determine how individuals with incomplete SCI performed in comparison to healthy subjects when they negotiate an inclined pathway. In addition, Sheehan and Gottschall (2012) demonstrated that slope and stair walking presented a greater fall risk than level walking in healthy individuals. Their results also showed a greater fall risk in slope walking compared to stair walking at similar angles. A greater fall risk during slope walking combined with difficulties producing lowerlimb joint powers and impairments in trunk control in individuals with incomplete SCI may limit their capacity to walk on an inclined pathway and increase the risk of injury. Therefore, the main objective of this study was to evaluate the impact of the SCI on the ability to walk uphill and downhill by comparing lower-limb gait cycle parameters and power generation and absorption between people with SCI and healthy subjects while walking on an inclined pathway. Specific objectives are to compare the values of the two groups of subjects 1) at natural gait speed (NGS) and 2) at matched speed; slow gait speed (SGS) for the healthy subjects and NGS for participants with SCI. We hypothesized that subjects with a SCI would present similar results to healthy subjects when the two groups walk at comparable speed. 2. Methods 2.1. Participants and clinical assessment A convenience sample of patients was recruited from the SCI rehabilitation unit of the Institut de readaptation Gingras-Lindsay de Montreal (IRGLM). Subjects were included in the study if they were able to walk
Table 1 Clinical characteristics. Clinical characteristics
Healthy participants (n = 11)
Participants with SCI (n = 11)
Mean
SD
Mean
SD
Age (yr) Height (m) Weight (kg) BMI (kg/m2)
50 1.68 68.6 24.1
14 0.10 12.1 2.3
50 1.71 77.4 26.2
15 0.08 15.3 3.59
Natural gait speed (m/s) Level walking Uphill walking Downhill walking
1.16 1.21 1.22
0.21 0.25 0.19
0.98 0.84 0.77
0.27 0.21 0.29
Slow gait speed (m/s) Level walking Uphill walking Downhill walking
0.82 0.92 0.95
0.13 0.19 0.16
on the inclined pathway (uphill and downhill) without walking aids, holding the rails or human assistance. Subjects were excluded if they had another disease in addition to the SCI (including a lower-limb or head trauma) or an insufficient tolerance level (b 120 min with rest). Ethics approval was obtained from the Research Ethics Committee of the Center for Interdisciplinary Research in Rehabilitation of Greater Montreal (CRIR 395-1108). Written consent was obtained after participants had read and understood the information about the research. A physical therapist evaluated every participant to obtain clinical characteristics. Clinical gait speeds (level, uphill and downhill walking) were measured over known distances: 3 m for level ground and 3.65 m for uphill and downhill walking (Table 1). Lower-limb strength was obtained using the Lower Extremity Motor Score (LEMS) of the ASIA Scale (maximal score of 25 by extremity) and balance was evaluated using the Berg Balance Scale (BBS, a maximal score of 56 indicated no balance deficit). According to a study, the BBS is a valid scale for evaluating balance in this population when combined with gait speed information (Lemay and Nadeau, 2010).
2.2. Experimentation Participants were invited to the Pathokinesiology laboratory, located on the 4th floor at IRGLM, for a 3-hour session and were asked to walk on the inclined pathway (uphill and downhill) at natural gait speed. Healthy subjects repeated the same tasks at slow gait speed (80% of natural gait speed). Between each trial, participants had the chance to take a rest. Participants executed a minimum of five trials for each condition, excluding the familiarization. The inclined pathway used in this study was 3.65 m long by 1.20 m wide and had a ramp of 8.5° (15%) (Fig. 1). A 1-m-long platform is annexed at the end of the pathway and handrails are placed on each side of the ramp for safety. Two AMTI® force plates are embedded in the middle of the inclined pathway to record forces and moments in three directions (x, y and z). Data were collected at a 600 Hz sampling frequency. There is no contact between the force plates and the inclined pathway so as to limit errors due to vibrations. These force plates have a ramp of 8.5° and were fixed on the ground before installing the inclined pathway. Four motion analysis cameras (60 Hz; Optotrak model 3020; NDI Technology Inc., Waterloo, Ontario, Canada) recorded the spatial position of 36 skin-fixed infrared light emitting diodes (LEDs) placed on the lower limbs, trunk and upper limbs (at least three LEDs on each major segment). A six-marker probe was used to define 26 bony landmarks to locate joint articulations relative to their segment. Kinetic and kinematic data were synced. An inverse dynamics analysis was performed using a link segment model, as defined by Winter (1991).
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
3
Fig. 1. Aluminum walkway with an inclined grade of 8.5° (15%) and a terminal level platform. An independent force platform support was designed to perfectly fit in its center.
2.3. Analysis Gait cycles were normalized (0–100%) and the trials were averaged for each participant and each condition to compare the results between groups. Data analysis included spatio-temporal parameters (gait speed, cadence and stride length) and kinetics (power). Data were obtained from the weaker (subjects with SCI) or the non-dominant lower limb (healthy subjects). The weaker lower limb was determined by the LEMS score and the dominant lower limb was determined as the leg used to take a step after a destabilizing force applied to the pelvis in the standing position (Sadeghi et al., 2000). Kinetic data were normalized to the mass of the participants. The main peak power values generally observed during level gait; maximal absorption and generation at the ankle (A1 and A2), the knee (K1, K2, K3, K4) and the hip (H1, H2 and H3), were then identified to compare the two groups. K4 and H2 correspond to absorption by the flexor muscles; A2, K2 and H1 to generation by the extensor muscles; A1, K1 and K3 to absorption by the extensor muscles and H3 to generation by the flexor muscles. Descriptive statistics were calculated and normality of the distribution was explored using the Shapiro–Wilk test. Independent sample t-tests or Mann–Whitney U tests were used to compare the lower-limb power values of the two groups of subjects 1) at natural gait speed (NGS) and 2) at matched speed; slow gait speed (SGS) for the healthy subjects and NGS for participants with SCI. All statistics were performed with SPSS Version 20 with the level of significance fixed at 0.05.
There were no significant differences in the clinical characteristics (age, weight, height and BMI) between the two groups (P N 0.05). Gait time–distance parameters of uphill and downhill walking for the two groups are shown in Fig. 2. Participants with SCI presented a reduced gait speed (uphill walking (Uw) and downhill walking (Dw): P = 0.000), cadence (Uw: P = 0.002; Dw: P = 0.016) and stride length (Uw and Dw: P = 0.000) compared to healthy subjects at NGS. There were no significant differences for these three parameters when healthy participants walked at SGS and participants with SCI at NGS (P N 0.067).
3.2. Lower-limb peak power values Profiles of the power values are shown in Figs. 3 and 4 with mean values of peak power reported in Table 2 for each condition. Participants with SCI presented lower power values at the ankle and at the knee compared to healthy subjects at NGS during uphill walking (A1: P = 0.011; A2: P = 0.000; K1: P = 0.008; K2: P = 0.020; K3: P = 0.045 and K4: P = 0.001). During downhill walking, participants with SCI showed a lower power at the ankle, knee and hip compared to healthy individuals at NGS (A2: P = 0.001; K1: P = 0.001; K2: P = 0.005; K3: P = 0.011; K4: P = 0.009 and H2: P = 0.023). When participants with SCI were compared to healthy individuals walking at SGS, the only significant differences were at the ankle for both uphill (A1: P = 0.044 and A2: P = 0.037) and downhill walking (A2: P = 0.010).
3. Results 4. Discussion 3.1. Participant demographics and gait cycle parameters Eleven participants with an AIS D SCI (10 men, 1 woman) and eleven healthy participants (6 men, 5 women), paired for age, height and weight, were recruited (Table 1). Six participants with SCI presented a traumatic SCI. The level of lesion varied from C1 to L3. Six of them had a cervical SCI, four a thoracic SCI and one a lumbar SCI. The mean (Standard deviation: SD) time post-lesion was 1.6 (2.2) years. The average score on the LEMS was 23 (2) on 25 for the right lower limb and 22 (3) on 25 for the left lower limb. Participants showed reduced balance, presenting a mean score of 53 (3) on 56 on the BBS and walked at a natural gait speed of 0.98 (0.27) m/s.
The main objective of this study was to compare lower-limb power values of SCI and healthy participants walking on an inclined pathway. Despite the recovery of a functional gait for the majority of AIS D individuals, clinical characteristics such as strength, spasticity and balance (Barbeau et al., 2006) may limit their ability to adapt to different environments and may restrict their community ambulation. Some studies have investigated the capacity of people with SCI to increase their gait speed but only a few have explored their capacity to do other walking tasks, such as walking on an inclined pathway. Therefore, it was pertinent to determine the strategy they use to adapt to inclined surfaces.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
4
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
Fig. 2. Gait cycle parameters: Gait speed (m/s); cadence (step/min); step length (m) during uphill (Uw) and downhill (Dw) walking. Diamonds correspond to healthy subjects at natural gait speed (NGS), triangles to subjects with SCI and squares to healthy subjects at slow gait speed (SGS).
4.1. Gait cycle parameters While walking on the inclined pathway, participants with SCI presented a reduced gait speed, cadence and stride length compared to healthy subjects also walking at their NGS. This is in agreement with other studies investigating gait characteristics of subjects with SCI
while walking on level ground (Barbeau et al., 2006; Kim et al., 2004). When the two groups were compared at similar gait speed, no differences were observed for these parameters. It is known that biomechanics are influenced by gait speed during walking (Roislien et al., 2009). The healthy subjects were therefore asked to walk at NGS and SGS to identify differences in the gait parameters that were specific to the
Uphill walking
Downhill walking
1.5
H1
1.5
1
1
H3
H3 0.5
0.5
H1
0
0
-0.5
-0.5
H2
H2
-1
-1 0
10
20
30
40
50
60
70
80
90
K2
1.5
0
100
1
1
0.5
0.5
0
0
-0.5
-0.5
K3
K1
-1
10
20
30
40
50
60
70
80
90
100
1.5
K2
-1
K4
K4
-1.5
-1.5
-2
-2
K3
-2.5
-2.5
K1
-3
-3 0
10
20
30
40
50
60
70
80
90
100
A2
3.5 3 2.5 2 1.5 1 0.5 0 -0.5 -1 -1.5
0
10
20
30
40
50
60
70
80
90
100
60
70
80
90
100
3.5 3 2.5
A2
2 1.5 1 0.5 0
A1
-0.5
A1
-1 -1.5 0
10
20
30
40
50
60
70
80
90
100
Fig. 3. Lower limb peak power values (W/kg) during uphill walking for the hip, knee and ankle. The continuous line corresponds to healthy subjects at natural gait speed (NGS); the dotted line to subjects with SCI and the dashed line to healthy subjects at slow gait speed (SGS).
0
10
20
30
40
50
Fig. 4. Lower limb peak power values (W/kg) during downhill walking for the hip, knee and ankle. The continuous line corresponds to healthy subjects at natural gait speed (NGS); the dotted line to subjects with SCI and the dashed line to healthy subjects at slow gait speed (SGS).
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
5
Table 2 Power peak values. Power peak values (W/kg)
Participants with SCI
Healthy participants at NGS
Healthy participants at SGS
Uphill
Mean
SD
Mean
SD
Mean
SD
Ankle A1 A2
−0.490 1.537
0.226 0.859
−0.250⁎ 3.386⁎
0.247 0.654
−0.279⁎⁎ 2.357⁎⁎
0.201 0.622
Knee K1 K2 K3 K4
−0.251 0.919 −0.420 −0.254
0.296 0.623 0.237 0.183
−0.685⁎ 1.423⁎ −0.686⁎ −0.568⁎
0.374 0.576 0.346 0.107
−0.275 0.899 −0.346 −0.308
0.232 0.606 0.158 0.095
Hip H1 H2 H3
0.957 −0.486 0.641
0.689 0.365 0.312
1.440 −0.683 0.852
0.561 0.302 0.366
0.829 −0.341 0.449
0.371 0.283 0.137
Downhill
Mean
SD
Mean
SD
Mean
SD
Ankle A1 A2
−0.896 0.935
0.451 0.611
−1.255 2.202⁎
0.311 0.622
−1.176 1.619⁎⁎
0.278 0.562
Knee K1 K2 K3 K4
−1.001 0.179 −1.296 −0.494
0.731 0.181 0.735 0.322
−2.886⁎ 0.599⁎ −2.108⁎ −0.904⁎
1.244 0.341 0.519 0.223
−1.360 0.256 −1.487 −0.472
0.927 0.242 0.395 0.154
Hip H1 H2 H3
0.181 −0.406 0.713
0.153 0.323 0.400
0.323 −0.797⁎ 0.967
0.391 0.381 0.644
0.185 −0.565 0.409
0.124 0.325 0.108
⁎ Significant differences between participants with SCI and healthy participants at natural gait speed (P b 0.05). ⁎⁎ Significant differences between participants with SCI and healthy participants at slow gait speed (P b 0.05).
injury. The participants with SCI recruited for this study presented a decreased gait speed compared to healthy individuals when walking on an inclined surface. Therefore, it was relevant to assess healthy subjects walking at slow speed to eliminate the confounding influence of the gait speed on the results when the two groups were compared. 4.2. Lower-limb power values Our results demonstrate that people with SCI present reduced lower-limb power values compared to healthy subjects walking at NGS. These differences are mainly due to the difference in gait speed of the two groups because, when participants with SCI were compared to healthy subjects walking at SGS, there were no differences in knee and hip power values. However, subjects with SCI still presented smaller power values at the ankle, even when the influence of speed was eliminated. These results suggest a greater motor deficit at the ankle or a preference not to use this muscle group, as revealed by the weak push-off (A2) at the end of the stance phase in uphill and downhill walking. Except for one participant who had a lumbar lesion (L3), all the participants recruited presented a cervical or a thoracic SCI lesion affecting their hip, knee and ankle muscles. The decreased power generation at the ankle agrees with the weaker push-off reported previously in studies investigating gait adaptations of individuals with SCI (Jayaraman et al., 2006; Leroux et al., 1999; Pepin et al., 2003). The hypothesis of a motor deficit of the plantar flexors is coherent with the findings of Jayaraman et al. (2006) who found that people with SCI present a lower isometric torque of the plantar flexor muscles compared to non-injured individuals. The group of participants recruited for Jayaraman et al.'s study presented an AIS C or AIS D SCI so they were more impaired than those recruited in the present study. In comparison to AIS D individuals, people with an AIS C SCI present a motor score b 3/5 for the majority of the muscles below the lesion (Scivoletto and Di Donna, 2009). Thus, despite a greater recovery, our participants still demonstrated lower ankle power values compared to the control
group. The results of Pepin et al. (2003) brought additional arguments in favor of a greater deficit at the ankle since they found that people with SCI had a limited capacity to increase their gait speed because there was no increase in plantar flexor electromyographic activity. Leroux et al. (1999) reported the same observation when subjects with SCI were asked to walk uphill. These two studies compared SCI participants to healthy subjects at matched gait speed to better identify deficits specific to the injury. In addition, these participants presented similar characteristics to those recruited in the current study. These studies corroborate the results previously presented and emphasize that the presence of a weaker push-off in this population might indicate that distal deficits are more extensive and do not disappear following rehabilitation. To compensate for this weak push-off, people with SCI might have presented a different pattern at the hip and knee, as reported by Leroux et al. (1999). According to Kim et al. (2004), hip muscle strength values are correlated with the community mobility of people with SCI. In a stroke population, Nadeau et al. (1999) demonstrated that the use of hip muscles may compensate for weak plantar flexors when there is an increase in gait speed. In the present study, we did not observe any compensation from the hip and knee power when people with SCI performed a challenging task such as walking uphill. Instead, the participants preferred to reduce the gait speed. Thus, our results emphasize the need to ask the individuals post-SCI to perform at higher speeds and to increase the utilization of their plantar flexors in doing so. This study presents some limitations. First, the comparison of the power values was limited to the weaker lower limb with the result that the between-side interactions were not assessed. Our participants did not have important clinical difference between sides, as revealed by the score at the Lower Extremity Motor Score (LEMS): right = 23/25 and left = 22/25. However, according to Kim et al. (2004), the strength of the less affected leg might be important for determining walking capacities. In future studies, it will be pertinent to assess the biomechanics of the two lower limbs and to analyze mechanical work. This latter might provide additional information regarding the
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
6
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
generation and absorption use in uphill and downhill walking. As an example the explanatory analysis done for downhill walking revealed that the mechanical work associated with H3 was significantly greater in individuals post-SCI compared to healthy subjects while the difference in the peak values did not differ between groups. The number of participants was small, reducing the ability to generalize our data to a large population. Moreover, considering the variability in the gait speed of individuals post-SCI, it might help to select more than one cadence of healthy subjects to match those of the patients, keeping in mind that the healthy “normal” gait pattern might be modified by the slow cadence imposed, even when familiarization trials preceded the gait recording. Finally, it would have been interesting to have a complete tableau of the impairments in electromyography and muscle strength. As suggested by Jayaraman et al. (2006), the ASIA score is based on manual muscle tests which present a ceiling effect and may be not sensitive enough to reveal more subtle deficits.
5 . Conclusions In conclusion, this study has demonstrated that, even with a good motor recovery, distal power deficits remain and may limit the subject's ability to adapt to uphill and downhill walking. Enhancing power production during plantar flexor activity may help increase the functional independence of this population.
Acknowledgments This work was financed by the Sensorimotor Rehabilitation Research Team (SMRRT; Strategic initiative, Canadian Institutes of Health Research — CIHR, #229269). Financial support to build the inclined pathway was provided by the Lindsay Foundation. Emilie Desrosiers was supported by a summer scholarship from the COPSE program (Faculty of Medicine, University of Montreal) and by the Fond de la Recherche du Québec en Santé (FRQ-S, #24943). Conflict of interest statement There is no conflict of interest for any of the authors.
Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.clinbiomech.2014.04.004.
References Barbeau, H., Nadeau, S., Garneau, C., 2006. Physical determinants, emerging concepts, and training approaches in gait of individuals with spinal cord injury. J. Neurotrauma 23, 571–585. Brotherton, S.S., Krause, J.S., Nietert, P.J., 2007. Falls in individuals with incomplete spinal cord injury. Spinal Cord 45, 37–40. Jayaraman, A., Gregory, C.M., Bowden, M., Stevens, J.E., Shah, P., Behrman, A.L., et al., 2006. Lower extremity skeletal muscle function in persons with incomplete spinal cord injury. Spinal Cord 44, 680–687. Kawamura, K., Tokuhiro, A., Takechi, H., 1991. Gait analysis of slope walking: a study on step length, stride width, time factors and deviation in the center of pressure. Acta Med. Okayama 45, 179–184. Kim, C.M., Eng, J.J., Whittaker, M.W., 2004. Level walking and ambulatory capacity in persons with incomplete spinal cord injury: relationship with muscle strength. Spinal Cord 42, 156–162. Kuster, M., Sakurai, S., Wood, G.A., 1995. Kinematic and kinetic comparison of downhill and level walking. Clin. Biomech. 10, 79–84. Lay, A.N., Hass, C.J., Gregor, R.J., 2006. The effects of sloped surfaces on locomotion: a kinematic and kinetic analysis. J. Biomech. 39, 1621–1628. Lay, A.N., Hass, C.J., Richard Nichols, T., Gregor, R.J., 2007. The effects of sloped surfaces on locomotion: an electromyographic analysis. J. Biomech. 40, 1276–1285. Lemay, J.F., Nadeau, S., 2010. Standing balance assessment in ASIA D paraplegic and tetraplegic participants: concurrent validity of the Berg Balance Scale. Spinal Cord 48, 245–250. Leroux, A., Fung, J., Barbeau, H., 1999. Adaptation of the walking pattern to uphill walking in normal and spinal-cord injured subjects. Exp. Brain Res. 126, 359–368. Leroux, A., Fung, J., Barbeau, H., 2002. Postural adaptation to walking on inclined surfaces: I. Normal strategies. Gait Posture 15, 64–74. Leroux, A., Fung, J., Barbeau, H., 2006. Postural adaptation to walking on inclined surfaces: II. Strategies following spinal cord injury. Clin. Neurophysiol. 117, 1273–1282. Nadeau, S., Gravel, D., Arsenault, A.B.., Bourbonnais, D., 1999. Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clin. Biomech. 14, 125–135. Noonan, V.K., Fingas, M., Farry, A., Baxter, D., Singh, A., Fehlings, M.G., et al., 2012. Incidence and prevalence of spinal cord injury in Canada: a national perspective. Neuroepidemiology 38, 219–226. Pepin, A., Norman, K.E., Barbeau, H., 2003. Treadmill walking in incomplete spinal-cordinjured subjects: 1. Adaptation to changes in speed. Spinal Cord 41, 257–270. Prentice, S.D., Hasler, E.N., Groves, J.J., Frank, J.S., 2004. Locomotor adaptations for changes in the slope of the walking surface. Gait Posture 20, 255–265. Roislien, J., Skare, O., Gustavsen, M., Broch, N.L., Rennie, L., Opheim, A., 2009. Simultaneous estimation of effects of gender, age and walking speed on kinematic gait data. Gait Posture 30, 441–445. Sadeghi, H., Allard, P., Prince, F., Labelle, H., 2000. Symmetry and limb dominance in ablebodied gait: a review. Gait Posture 12, 34–45. Scivoletto, G., Di Donna, V., 2009. Prediction of walking recovery after spinal cord injury. Brain Res. Bull. 78, 43–51. Scivoletto, G., Romanelli, A., Mariotti, A., Marinucci, D., Tamburella, F., Mammone, A., et al., 2008. Clinical factors that affect walking level and performance in chronic spinal cord lesion patients. Spine (Phila Pa 1976) 33, 259–264. Sheehan, R.C., Gottschall, J.S., 2012. At similar angles, slope walking has a greater fall risk than stair walking. Appl. Ergon. 43, 473–478. Whiteneck, G.G., Charlifue, S.W., Frankel, H.L., Fraser, M.H., Gardner, B.P., Gerhart, K.A., et al., 1992. Mortality, morbidity, and psychosocial outcomes of persons spinal cord injured more than 20 years ago. Paraplegia 30, 617–630. Winter, D.A., 1991. The Biomechanics and Motor Control of Human Gait: Normal, Elderly and Pathological. University of Waterloo Press, Waterloo, Ont.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Gait adaptation during walking on an inclined pathway following spinal cord injury Emilie Desrosiers a,⁎, Cyril Duclos a,b, Sylvie Nadeau a,b a b
School of rehabilitation, Faculty of medicine, Universite de Montreal, Montreal, Canada Laboratoire de pathokinesiologie, Centre de recherche interdisciplinaire en readaptation (CRIR), Institut de readaptation Gingras-Lindsay-de-Montreal, Montreal, Quebec, Canada
a r t i c l e
i n f o
Article history: Received 2 December 2013 Accepted 8 April 2014 Keywords: Gait adaptation Inclined pathway Biomechanics Spinal cord injury Rehabilitation
a b s t r a c t Background: Individuals with incomplete spinal cord injury need to be assessed in different environments. The objective of this study was to compare lower-limb power generation in subjects with spinal cord injury and healthy subjects while walking on an inclined pathway. Methods: Eleven subjects with spinal cord injury and eleven healthy subjects walked on an inclined pathway at their natural gait speed and at slow gait speed (healthy subjects only). Ground reaction forces were recorded by force plates embedded in the inclined pathway and a 3-D motion analysis system recorded lower-limb motions. Data analysis included gait cycle parameters and joint peak powers. Differences were identified by student t-tests. Findings: Gait cycle parameters were lower in spinal cord injury subjects compared to healthy subjects at natural speed but similar at slow gait speed. Subjects with spinal cord injury presented lower power at the ankle, knee and hip compared to healthy subjects at natural gait speed while only the power generation at push-off remained lower when the two groups performed at similar speed. Interpretation: The most important differences are associated with the fact that individuals with spinal cord injury walk at a slower speed, except for the ankle power generation. This study demonstrated that, even with a good motor recovery, distal deficits remain and may limit the ability to adapt to uphill and downhill walking. Inclined pathways are indicated to train patients with spinal cord injury. Clinicians should focus on the speed of uphill and downhill walking and on the use of plantar flexors. © 2014 Elsevier Ltd. All rights reserved.
1. Introduction Recent medical progress has allowed an increase in the survival and functional independence of people following a spinal cord injury (SCI) (Whiteneck et al., 1992). Recovering independent walk is one of the main goals of individuals with SCI, especially in people with an incomplete lesion (Scivoletto and Di Donna, 2009). About 80 to 100% of AIS D individuals will recover the ability to walk one year post injury (Lemay and Nadeau, 2010). A person is classified as AIS D if the majority of muscles below the lesion have a motor score ≥3/5 according to the American Spinal Injury Association (ASIA) Scale (Scivoletto and Di Donna, 2009). A score ≥ 3/5 indicates that the muscle has the capacity to counteract gravity. The cause and severity of the SCI will have a major influence on the rehabilitation and the capacity to walk (Noonan et al., 2012). Despite a functional recovery of walk, many limitations such as a decrease in gait speed and endurance may remain following rehabilitation (Kim et al., 2004).
⁎ Corresponding author at: Laboratoire de pathokinesiologie, Centre de recherche interdisciplinaire en readaptation du Montreal metropolitain, Institut de readaptation Gingras-Lindsay-de-Montreal, 6300 Avenue Darlington, Montreal, Quebec H3S 2J4, Canada. E-mail address: [email protected] (E. Desrosiers).
Walking is a complex task that requires sufficient muscle strength, balance and coordination (Barbeau et al., 2006). For people with SCI, the strength of the leg muscles, particularly knee extensors and hip muscles, seems to be one of the principal factors that can predict their capacity to recover a functional walk (Barbeau et al., 2006; Kim et al., 2004). Meanwhile, other clinical factors such as spasticity, posture, cocontractions and loss of proprioception can limit the ability to walk (Barbeau et al., 2006; Brotherton et al., 2007; Leroux et al., 1999; Scivoletto et al., 2008). In addition to a decrease in step length and an increase in double time support in comparison to healthy individuals (Barbeau et al., 2006), subjects with SCI who are able to walk also present an increased knee flexion and an abnormal knee–hip coordination compared to healthy subjects (Leroux et al., 1999). Changes in muscular activation may limit their capacity to adapt their gait in different environments (Leroux et al., 1999). Moreover, the use of walking aids is frequent in this population to assist with negotiation of the environment. However, it also may increase energy expenditure and alter posture (Leroux et al., 2006). Walking on an inclined pathway requires changes in motor strategies to adapt to the ramp (Lay et al., 2006). During uphill walking, healthy subjects reduce their cadence (Prentice et al., 2004) and increase their step length (Kawamura et al., 1991; Leroux et al., 2002). There is also an increase in knee flexion at heel strike and an increased
http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004 0268-0033/© 2014 Elsevier Ltd. All rights reserved.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
2
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
leg extension during the stance phase (Lay et al., 2006) along with an increase in propulsion (Lay et al., 2006; Leroux et al., 2002) and in hip extensor and plantar flexor moments (Lay et al., 2007). During downhill walking, healthy subjects decrease their step length (Kuster et al., 1995; Leroux et al., 2002) and increase their cadence (Kawamura et al., 1991; Kuster et al., 1995; Lay et al., 2006). Healthy subjects also show an increase in their knee flexion during the stance phase (Lay et al., 2006; Leroux et al., 2002), knee extensors and dorsiflexor activity (Kuster et al., 1995; Lay et al., 2007) and breaking force (Lay et al., 2006, 2007). Few studies have quantified the adaptation of subjects with SCI walking on an inclined pathway. Their capacity to adapt to inclined surfaces seems to be correlated with their gait speed during level walking (Leroux et al., 1999, 2006). During uphill walking, subjects with SCI present an increase in hip and trunk flexion and a weak push-off at the end of the stance phase (Leroux et al., 1999). This constant trunk flexion position minimizes the gravity effect on the knee extensors during uphill walking but might reduce the capacity to adapt to downhill walking (Leroux et al., 2006). In fact, a normal adaptation is to present a backward tilt of the trunk as the descending slope increases (Leroux et al., 2002). With regard to these results, this population seems to present impaired adaptations to inclined walking which can lead to a loss of balance and an inefficient gait pattern characterized by a decreased walking speed. Authors agree that more studies are necessary to increase our understanding of the walking adaptation of people with SCI in more challenging environments to optimize their rehabilitation. Jayaraman et al. (2006) demonstrated that individuals with incomplete SCI presented deficits in generating peak isometric torque in the knee extensor and plantar flexor muscle groups during a voluntary contraction. Considering the role of the ankle in propulsion during walking, the difficulty in generating an adequate push-off could have a functional impact on their gait abilities. In addition, individuals with SCI generally present a decrease in angular excursion, reducing their capacity to produce high angular velocities and, consequently, decreasing lower-limb power values (Barbeau et al., 2006). Thus, because of the changes in kinetics and the frequent occurrence of uphill and downhill walking in daily living, it is necessary to determine how individuals with incomplete SCI performed in comparison to healthy subjects when they negotiate an inclined pathway. In addition, Sheehan and Gottschall (2012) demonstrated that slope and stair walking presented a greater fall risk than level walking in healthy individuals. Their results also showed a greater fall risk in slope walking compared to stair walking at similar angles. A greater fall risk during slope walking combined with difficulties producing lowerlimb joint powers and impairments in trunk control in individuals with incomplete SCI may limit their capacity to walk on an inclined pathway and increase the risk of injury. Therefore, the main objective of this study was to evaluate the impact of the SCI on the ability to walk uphill and downhill by comparing lower-limb gait cycle parameters and power generation and absorption between people with SCI and healthy subjects while walking on an inclined pathway. Specific objectives are to compare the values of the two groups of subjects 1) at natural gait speed (NGS) and 2) at matched speed; slow gait speed (SGS) for the healthy subjects and NGS for participants with SCI. We hypothesized that subjects with a SCI would present similar results to healthy subjects when the two groups walk at comparable speed. 2. Methods 2.1. Participants and clinical assessment A convenience sample of patients was recruited from the SCI rehabilitation unit of the Institut de readaptation Gingras-Lindsay de Montreal (IRGLM). Subjects were included in the study if they were able to walk
Table 1 Clinical characteristics. Clinical characteristics
Healthy participants (n = 11)
Participants with SCI (n = 11)
Mean
SD
Mean
SD
Age (yr) Height (m) Weight (kg) BMI (kg/m2)
50 1.68 68.6 24.1
14 0.10 12.1 2.3
50 1.71 77.4 26.2
15 0.08 15.3 3.59
Natural gait speed (m/s) Level walking Uphill walking Downhill walking
1.16 1.21 1.22
0.21 0.25 0.19
0.98 0.84 0.77
0.27 0.21 0.29
Slow gait speed (m/s) Level walking Uphill walking Downhill walking
0.82 0.92 0.95
0.13 0.19 0.16
on the inclined pathway (uphill and downhill) without walking aids, holding the rails or human assistance. Subjects were excluded if they had another disease in addition to the SCI (including a lower-limb or head trauma) or an insufficient tolerance level (b 120 min with rest). Ethics approval was obtained from the Research Ethics Committee of the Center for Interdisciplinary Research in Rehabilitation of Greater Montreal (CRIR 395-1108). Written consent was obtained after participants had read and understood the information about the research. A physical therapist evaluated every participant to obtain clinical characteristics. Clinical gait speeds (level, uphill and downhill walking) were measured over known distances: 3 m for level ground and 3.65 m for uphill and downhill walking (Table 1). Lower-limb strength was obtained using the Lower Extremity Motor Score (LEMS) of the ASIA Scale (maximal score of 25 by extremity) and balance was evaluated using the Berg Balance Scale (BBS, a maximal score of 56 indicated no balance deficit). According to a study, the BBS is a valid scale for evaluating balance in this population when combined with gait speed information (Lemay and Nadeau, 2010).
2.2. Experimentation Participants were invited to the Pathokinesiology laboratory, located on the 4th floor at IRGLM, for a 3-hour session and were asked to walk on the inclined pathway (uphill and downhill) at natural gait speed. Healthy subjects repeated the same tasks at slow gait speed (80% of natural gait speed). Between each trial, participants had the chance to take a rest. Participants executed a minimum of five trials for each condition, excluding the familiarization. The inclined pathway used in this study was 3.65 m long by 1.20 m wide and had a ramp of 8.5° (15%) (Fig. 1). A 1-m-long platform is annexed at the end of the pathway and handrails are placed on each side of the ramp for safety. Two AMTI® force plates are embedded in the middle of the inclined pathway to record forces and moments in three directions (x, y and z). Data were collected at a 600 Hz sampling frequency. There is no contact between the force plates and the inclined pathway so as to limit errors due to vibrations. These force plates have a ramp of 8.5° and were fixed on the ground before installing the inclined pathway. Four motion analysis cameras (60 Hz; Optotrak model 3020; NDI Technology Inc., Waterloo, Ontario, Canada) recorded the spatial position of 36 skin-fixed infrared light emitting diodes (LEDs) placed on the lower limbs, trunk and upper limbs (at least three LEDs on each major segment). A six-marker probe was used to define 26 bony landmarks to locate joint articulations relative to their segment. Kinetic and kinematic data were synced. An inverse dynamics analysis was performed using a link segment model, as defined by Winter (1991).
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
3
Fig. 1. Aluminum walkway with an inclined grade of 8.5° (15%) and a terminal level platform. An independent force platform support was designed to perfectly fit in its center.
2.3. Analysis Gait cycles were normalized (0–100%) and the trials were averaged for each participant and each condition to compare the results between groups. Data analysis included spatio-temporal parameters (gait speed, cadence and stride length) and kinetics (power). Data were obtained from the weaker (subjects with SCI) or the non-dominant lower limb (healthy subjects). The weaker lower limb was determined by the LEMS score and the dominant lower limb was determined as the leg used to take a step after a destabilizing force applied to the pelvis in the standing position (Sadeghi et al., 2000). Kinetic data were normalized to the mass of the participants. The main peak power values generally observed during level gait; maximal absorption and generation at the ankle (A1 and A2), the knee (K1, K2, K3, K4) and the hip (H1, H2 and H3), were then identified to compare the two groups. K4 and H2 correspond to absorption by the flexor muscles; A2, K2 and H1 to generation by the extensor muscles; A1, K1 and K3 to absorption by the extensor muscles and H3 to generation by the flexor muscles. Descriptive statistics were calculated and normality of the distribution was explored using the Shapiro–Wilk test. Independent sample t-tests or Mann–Whitney U tests were used to compare the lower-limb power values of the two groups of subjects 1) at natural gait speed (NGS) and 2) at matched speed; slow gait speed (SGS) for the healthy subjects and NGS for participants with SCI. All statistics were performed with SPSS Version 20 with the level of significance fixed at 0.05.
There were no significant differences in the clinical characteristics (age, weight, height and BMI) between the two groups (P N 0.05). Gait time–distance parameters of uphill and downhill walking for the two groups are shown in Fig. 2. Participants with SCI presented a reduced gait speed (uphill walking (Uw) and downhill walking (Dw): P = 0.000), cadence (Uw: P = 0.002; Dw: P = 0.016) and stride length (Uw and Dw: P = 0.000) compared to healthy subjects at NGS. There were no significant differences for these three parameters when healthy participants walked at SGS and participants with SCI at NGS (P N 0.067).
3.2. Lower-limb peak power values Profiles of the power values are shown in Figs. 3 and 4 with mean values of peak power reported in Table 2 for each condition. Participants with SCI presented lower power values at the ankle and at the knee compared to healthy subjects at NGS during uphill walking (A1: P = 0.011; A2: P = 0.000; K1: P = 0.008; K2: P = 0.020; K3: P = 0.045 and K4: P = 0.001). During downhill walking, participants with SCI showed a lower power at the ankle, knee and hip compared to healthy individuals at NGS (A2: P = 0.001; K1: P = 0.001; K2: P = 0.005; K3: P = 0.011; K4: P = 0.009 and H2: P = 0.023). When participants with SCI were compared to healthy individuals walking at SGS, the only significant differences were at the ankle for both uphill (A1: P = 0.044 and A2: P = 0.037) and downhill walking (A2: P = 0.010).
3. Results 4. Discussion 3.1. Participant demographics and gait cycle parameters Eleven participants with an AIS D SCI (10 men, 1 woman) and eleven healthy participants (6 men, 5 women), paired for age, height and weight, were recruited (Table 1). Six participants with SCI presented a traumatic SCI. The level of lesion varied from C1 to L3. Six of them had a cervical SCI, four a thoracic SCI and one a lumbar SCI. The mean (Standard deviation: SD) time post-lesion was 1.6 (2.2) years. The average score on the LEMS was 23 (2) on 25 for the right lower limb and 22 (3) on 25 for the left lower limb. Participants showed reduced balance, presenting a mean score of 53 (3) on 56 on the BBS and walked at a natural gait speed of 0.98 (0.27) m/s.
The main objective of this study was to compare lower-limb power values of SCI and healthy participants walking on an inclined pathway. Despite the recovery of a functional gait for the majority of AIS D individuals, clinical characteristics such as strength, spasticity and balance (Barbeau et al., 2006) may limit their ability to adapt to different environments and may restrict their community ambulation. Some studies have investigated the capacity of people with SCI to increase their gait speed but only a few have explored their capacity to do other walking tasks, such as walking on an inclined pathway. Therefore, it was pertinent to determine the strategy they use to adapt to inclined surfaces.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
4
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
Fig. 2. Gait cycle parameters: Gait speed (m/s); cadence (step/min); step length (m) during uphill (Uw) and downhill (Dw) walking. Diamonds correspond to healthy subjects at natural gait speed (NGS), triangles to subjects with SCI and squares to healthy subjects at slow gait speed (SGS).
4.1. Gait cycle parameters While walking on the inclined pathway, participants with SCI presented a reduced gait speed, cadence and stride length compared to healthy subjects also walking at their NGS. This is in agreement with other studies investigating gait characteristics of subjects with SCI
while walking on level ground (Barbeau et al., 2006; Kim et al., 2004). When the two groups were compared at similar gait speed, no differences were observed for these parameters. It is known that biomechanics are influenced by gait speed during walking (Roislien et al., 2009). The healthy subjects were therefore asked to walk at NGS and SGS to identify differences in the gait parameters that were specific to the
Uphill walking
Downhill walking
1.5
H1
1.5
1
1
H3
H3 0.5
0.5
H1
0
0
-0.5
-0.5
H2
H2
-1
-1 0
10
20
30
40
50
60
70
80
90
K2
1.5
0
100
1
1
0.5
0.5
0
0
-0.5
-0.5
K3
K1
-1
10
20
30
40
50
60
70
80
90
100
1.5
K2
-1
K4
K4
-1.5
-1.5
-2
-2
K3
-2.5
-2.5
K1
-3
-3 0
10
20
30
40
50
60
70
80
90
100
A2
3.5 3 2.5 2 1.5 1 0.5 0 -0.5 -1 -1.5
0
10
20
30
40
50
60
70
80
90
100
60
70
80
90
100
3.5 3 2.5
A2
2 1.5 1 0.5 0
A1
-0.5
A1
-1 -1.5 0
10
20
30
40
50
60
70
80
90
100
Fig. 3. Lower limb peak power values (W/kg) during uphill walking for the hip, knee and ankle. The continuous line corresponds to healthy subjects at natural gait speed (NGS); the dotted line to subjects with SCI and the dashed line to healthy subjects at slow gait speed (SGS).
0
10
20
30
40
50
Fig. 4. Lower limb peak power values (W/kg) during downhill walking for the hip, knee and ankle. The continuous line corresponds to healthy subjects at natural gait speed (NGS); the dotted line to subjects with SCI and the dashed line to healthy subjects at slow gait speed (SGS).
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
5
Table 2 Power peak values. Power peak values (W/kg)
Participants with SCI
Healthy participants at NGS
Healthy participants at SGS
Uphill
Mean
SD
Mean
SD
Mean
SD
Ankle A1 A2
−0.490 1.537
0.226 0.859
−0.250⁎ 3.386⁎
0.247 0.654
−0.279⁎⁎ 2.357⁎⁎
0.201 0.622
Knee K1 K2 K3 K4
−0.251 0.919 −0.420 −0.254
0.296 0.623 0.237 0.183
−0.685⁎ 1.423⁎ −0.686⁎ −0.568⁎
0.374 0.576 0.346 0.107
−0.275 0.899 −0.346 −0.308
0.232 0.606 0.158 0.095
Hip H1 H2 H3
0.957 −0.486 0.641
0.689 0.365 0.312
1.440 −0.683 0.852
0.561 0.302 0.366
0.829 −0.341 0.449
0.371 0.283 0.137
Downhill
Mean
SD
Mean
SD
Mean
SD
Ankle A1 A2
−0.896 0.935
0.451 0.611
−1.255 2.202⁎
0.311 0.622
−1.176 1.619⁎⁎
0.278 0.562
Knee K1 K2 K3 K4
−1.001 0.179 −1.296 −0.494
0.731 0.181 0.735 0.322
−2.886⁎ 0.599⁎ −2.108⁎ −0.904⁎
1.244 0.341 0.519 0.223
−1.360 0.256 −1.487 −0.472
0.927 0.242 0.395 0.154
Hip H1 H2 H3
0.181 −0.406 0.713
0.153 0.323 0.400
0.323 −0.797⁎ 0.967
0.391 0.381 0.644
0.185 −0.565 0.409
0.124 0.325 0.108
⁎ Significant differences between participants with SCI and healthy participants at natural gait speed (P b 0.05). ⁎⁎ Significant differences between participants with SCI and healthy participants at slow gait speed (P b 0.05).
injury. The participants with SCI recruited for this study presented a decreased gait speed compared to healthy individuals when walking on an inclined surface. Therefore, it was relevant to assess healthy subjects walking at slow speed to eliminate the confounding influence of the gait speed on the results when the two groups were compared. 4.2. Lower-limb power values Our results demonstrate that people with SCI present reduced lower-limb power values compared to healthy subjects walking at NGS. These differences are mainly due to the difference in gait speed of the two groups because, when participants with SCI were compared to healthy subjects walking at SGS, there were no differences in knee and hip power values. However, subjects with SCI still presented smaller power values at the ankle, even when the influence of speed was eliminated. These results suggest a greater motor deficit at the ankle or a preference not to use this muscle group, as revealed by the weak push-off (A2) at the end of the stance phase in uphill and downhill walking. Except for one participant who had a lumbar lesion (L3), all the participants recruited presented a cervical or a thoracic SCI lesion affecting their hip, knee and ankle muscles. The decreased power generation at the ankle agrees with the weaker push-off reported previously in studies investigating gait adaptations of individuals with SCI (Jayaraman et al., 2006; Leroux et al., 1999; Pepin et al., 2003). The hypothesis of a motor deficit of the plantar flexors is coherent with the findings of Jayaraman et al. (2006) who found that people with SCI present a lower isometric torque of the plantar flexor muscles compared to non-injured individuals. The group of participants recruited for Jayaraman et al.'s study presented an AIS C or AIS D SCI so they were more impaired than those recruited in the present study. In comparison to AIS D individuals, people with an AIS C SCI present a motor score b 3/5 for the majority of the muscles below the lesion (Scivoletto and Di Donna, 2009). Thus, despite a greater recovery, our participants still demonstrated lower ankle power values compared to the control
group. The results of Pepin et al. (2003) brought additional arguments in favor of a greater deficit at the ankle since they found that people with SCI had a limited capacity to increase their gait speed because there was no increase in plantar flexor electromyographic activity. Leroux et al. (1999) reported the same observation when subjects with SCI were asked to walk uphill. These two studies compared SCI participants to healthy subjects at matched gait speed to better identify deficits specific to the injury. In addition, these participants presented similar characteristics to those recruited in the current study. These studies corroborate the results previously presented and emphasize that the presence of a weaker push-off in this population might indicate that distal deficits are more extensive and do not disappear following rehabilitation. To compensate for this weak push-off, people with SCI might have presented a different pattern at the hip and knee, as reported by Leroux et al. (1999). According to Kim et al. (2004), hip muscle strength values are correlated with the community mobility of people with SCI. In a stroke population, Nadeau et al. (1999) demonstrated that the use of hip muscles may compensate for weak plantar flexors when there is an increase in gait speed. In the present study, we did not observe any compensation from the hip and knee power when people with SCI performed a challenging task such as walking uphill. Instead, the participants preferred to reduce the gait speed. Thus, our results emphasize the need to ask the individuals post-SCI to perform at higher speeds and to increase the utilization of their plantar flexors in doing so. This study presents some limitations. First, the comparison of the power values was limited to the weaker lower limb with the result that the between-side interactions were not assessed. Our participants did not have important clinical difference between sides, as revealed by the score at the Lower Extremity Motor Score (LEMS): right = 23/25 and left = 22/25. However, according to Kim et al. (2004), the strength of the less affected leg might be important for determining walking capacities. In future studies, it will be pertinent to assess the biomechanics of the two lower limbs and to analyze mechanical work. This latter might provide additional information regarding the
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
6
E. Desrosiers et al. / Clinical Biomechanics xxx (2014) xxx–xxx
generation and absorption use in uphill and downhill walking. As an example the explanatory analysis done for downhill walking revealed that the mechanical work associated with H3 was significantly greater in individuals post-SCI compared to healthy subjects while the difference in the peak values did not differ between groups. The number of participants was small, reducing the ability to generalize our data to a large population. Moreover, considering the variability in the gait speed of individuals post-SCI, it might help to select more than one cadence of healthy subjects to match those of the patients, keeping in mind that the healthy “normal” gait pattern might be modified by the slow cadence imposed, even when familiarization trials preceded the gait recording. Finally, it would have been interesting to have a complete tableau of the impairments in electromyography and muscle strength. As suggested by Jayaraman et al. (2006), the ASIA score is based on manual muscle tests which present a ceiling effect and may be not sensitive enough to reveal more subtle deficits.
5 . Conclusions In conclusion, this study has demonstrated that, even with a good motor recovery, distal power deficits remain and may limit the subject's ability to adapt to uphill and downhill walking. Enhancing power production during plantar flexor activity may help increase the functional independence of this population.
Acknowledgments This work was financed by the Sensorimotor Rehabilitation Research Team (SMRRT; Strategic initiative, Canadian Institutes of Health Research — CIHR, #229269). Financial support to build the inclined pathway was provided by the Lindsay Foundation. Emilie Desrosiers was supported by a summer scholarship from the COPSE program (Faculty of Medicine, University of Montreal) and by the Fond de la Recherche du Québec en Santé (FRQ-S, #24943). Conflict of interest statement There is no conflict of interest for any of the authors.
Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.clinbiomech.2014.04.004.
References Barbeau, H., Nadeau, S., Garneau, C., 2006. Physical determinants, emerging concepts, and training approaches in gait of individuals with spinal cord injury. J. Neurotrauma 23, 571–585. Brotherton, S.S., Krause, J.S., Nietert, P.J., 2007. Falls in individuals with incomplete spinal cord injury. Spinal Cord 45, 37–40. Jayaraman, A., Gregory, C.M., Bowden, M., Stevens, J.E., Shah, P., Behrman, A.L., et al., 2006. Lower extremity skeletal muscle function in persons with incomplete spinal cord injury. Spinal Cord 44, 680–687. Kawamura, K., Tokuhiro, A., Takechi, H., 1991. Gait analysis of slope walking: a study on step length, stride width, time factors and deviation in the center of pressure. Acta Med. Okayama 45, 179–184. Kim, C.M., Eng, J.J., Whittaker, M.W., 2004. Level walking and ambulatory capacity in persons with incomplete spinal cord injury: relationship with muscle strength. Spinal Cord 42, 156–162. Kuster, M., Sakurai, S., Wood, G.A., 1995. Kinematic and kinetic comparison of downhill and level walking. Clin. Biomech. 10, 79–84. Lay, A.N., Hass, C.J., Gregor, R.J., 2006. The effects of sloped surfaces on locomotion: a kinematic and kinetic analysis. J. Biomech. 39, 1621–1628. Lay, A.N., Hass, C.J., Richard Nichols, T., Gregor, R.J., 2007. The effects of sloped surfaces on locomotion: an electromyographic analysis. J. Biomech. 40, 1276–1285. Lemay, J.F., Nadeau, S., 2010. Standing balance assessment in ASIA D paraplegic and tetraplegic participants: concurrent validity of the Berg Balance Scale. Spinal Cord 48, 245–250. Leroux, A., Fung, J., Barbeau, H., 1999. Adaptation of the walking pattern to uphill walking in normal and spinal-cord injured subjects. Exp. Brain Res. 126, 359–368. Leroux, A., Fung, J., Barbeau, H., 2002. Postural adaptation to walking on inclined surfaces: I. Normal strategies. Gait Posture 15, 64–74. Leroux, A., Fung, J., Barbeau, H., 2006. Postural adaptation to walking on inclined surfaces: II. Strategies following spinal cord injury. Clin. Neurophysiol. 117, 1273–1282. Nadeau, S., Gravel, D., Arsenault, A.B.., Bourbonnais, D., 1999. Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clin. Biomech. 14, 125–135. Noonan, V.K., Fingas, M., Farry, A., Baxter, D., Singh, A., Fehlings, M.G., et al., 2012. Incidence and prevalence of spinal cord injury in Canada: a national perspective. Neuroepidemiology 38, 219–226. Pepin, A., Norman, K.E., Barbeau, H., 2003. Treadmill walking in incomplete spinal-cordinjured subjects: 1. Adaptation to changes in speed. Spinal Cord 41, 257–270. Prentice, S.D., Hasler, E.N., Groves, J.J., Frank, J.S., 2004. Locomotor adaptations for changes in the slope of the walking surface. Gait Posture 20, 255–265. Roislien, J., Skare, O., Gustavsen, M., Broch, N.L., Rennie, L., Opheim, A., 2009. Simultaneous estimation of effects of gender, age and walking speed on kinematic gait data. Gait Posture 30, 441–445. Sadeghi, H., Allard, P., Prince, F., Labelle, H., 2000. Symmetry and limb dominance in ablebodied gait: a review. Gait Posture 12, 34–45. Scivoletto, G., Di Donna, V., 2009. Prediction of walking recovery after spinal cord injury. Brain Res. Bull. 78, 43–51. Scivoletto, G., Romanelli, A., Mariotti, A., Marinucci, D., Tamburella, F., Mammone, A., et al., 2008. Clinical factors that affect walking level and performance in chronic spinal cord lesion patients. Spine (Phila Pa 1976) 33, 259–264. Sheehan, R.C., Gottschall, J.S., 2012. At similar angles, slope walking has a greater fall risk than stair walking. Appl. Ergon. 43, 473–478. Whiteneck, G.G., Charlifue, S.W., Frankel, H.L., Fraser, M.H., Gardner, B.P., Gerhart, K.A., et al., 1992. Mortality, morbidity, and psychosocial outcomes of persons spinal cord injured more than 20 years ago. Paraplegia 30, 617–630. Winter, D.A., 1991. The Biomechanics and Motor Control of Human Gait: Normal, Elderly and Pathological. University of Waterloo Press, Waterloo, Ont.
Please cite this article as: Desrosiers, E., et al., Gait adaptation during walking on an inclined pathway following spinal cord injury, Clin. Biomech. (2014), http://dx.doi.org/10.1016/j.clinbiomech.2014.04.004
