Accepted Manuscript Postural and dynamic balance while walking in adults with an incomplete spinal cord injury Jean-François Lemay, Cyril Duclos, Sylvie Nadeau, Dany Gagnon, Émilie Desrosiers PII: DOI: Reference:
S1050-6411(14)00077-7 http://dx.doi.org/10.1016/j.jelekin.2014.04.013 JJEK 1706
To appear in:
Journal of Electromyography and Kinesiology
Received Date: Revised Date: Accepted Date:
28 October 2013 19 March 2014 17 April 2014
Please cite this article as: J-F. Lemay, C. Duclos, S. Nadeau, D. Gagnon, É. Desrosiers, Postural and dynamic balance while walking in adults with an incomplete spinal cord injury, Journal of Electromyography and Kinesiology (2014), doi: http://dx.doi.org/10.1016/j.jelekin.2014.04.013
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Journal of Electromyography and Kinesiology
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Original Article
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Postural and dynamic balance while walking in adults with an incomplete spinal
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cord injury.
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Jean-François Lemaya,b, Cyril Duclosa,b, Sylvie Nadeaua,b, Dany Gagnona,b, Émilie
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Desrosiersb.
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a
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b
School of Rehabilitation (www.readap.umontreal.ca), Université de Montréal, Montreal, Canada Pathokinesiology Laboratory (www.pathokin.ca), Centre for Interdisciplinary Research in Rehabilitation of Greater Montreal — Institut de réadaptation Gingras-Lindsay de Montréal, Montreal, Canada
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Jean-François Lemay is supported by a doctoral scholarship from the Fonds de la recherche du Québec-Santé (FRQS). Dany Gagnon holds a Junior 1 Award from the FRQS. Cyril Duclos, Sylvie Nadeau and Dany Gagnon are members of the QuebecOntario Spinal Cord Injury Research Team and the SensoriMotor Rehabilitation Research Team. The equipment and material required to complete this project at the Pathokinesiology Laboratory was financed in part by the Canada Foundation for Innovation. This project was funded in part by a research grant from the Craig H. Neilson Foundation.
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Corresponding author:
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Jean-François Lemay, Centre for Interdisciplinary Research in Rehabilitation of Greater Montreal – Institut de réadaptation Gingras-Lindsay-de-Montréal, Pathokinesiology Laboratory, 6300 avenue Darlington, Montreal, QC, Canada H3S 2J4. E-mail:
[email protected] 28 29
Keywords:
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Gait; biomechanics; balance; rehabilitation; spinal cord injury.
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Abstract: 218 words
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Manuscript: 4250 words (4400 max)
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Tables and figures: 6
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Introduction
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Following a spinal cord injury, individuals commonly mention recovery of walking
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function as one of the most important goals of rehabilitation (Ditunno et al., 2008). The
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prognosis of independent walking among people with an incomplete spinal cord injury
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(ISCI) (American Spinal Injury Association Impairment Scale (AIS), level D), being
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greater than 80%, supports the likelihood of reaching this goal (Scivoletto et al., 2009).
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In addition to impaired walking abilities, an ISCI disrupts the normal flow of sensory and
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motor information involved in balance control (Barbeau et al., 1999). Standing balance is
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indeed considered a major determinant of walking abilities (Barbeau et al., 2006,
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Scivoletto et al., 2008) and is associated with walking speed and the use of ambulatory
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assistive devices in this population (Lemay and Nadeau, 2009, Wirz et al., 2010).
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Balance impairments may also partly explain the high incidence of falls in this population
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(39-75% according to various studies (Amatachaya et al., 2011, Brotherton et al., 2007,
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Phonthee et al., 2013)) and resulting secondary fall-related complications, such as
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fractures and decreased social participation (Amatachaya et al., 2011, Brotherton et al.,
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2007, Phonthee et al., 2013).
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To date, few studies have quantified balance during gait in individuals with SCI. Day et
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al. (2011) documented greater variability in step width and step length, margin of stability
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as well as anteroposterior and mediolateral foot placement compared to able-bodied
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individuals while walking on a treadmill (Day et al., 2011). Moreover, variability in step
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length and foot placement was significantly and negatively associated with the Berg
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Balance Scale, a clinical measure of balance (Berg et al., 1989). Leroux et al. (2006)
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previously reported postural modification including accentuated trunk flexion and forward
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pelvic tilt in individuals with an ISCI while walking on a treadmill as the grades of
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inclination were increased, presumably to compensate for decreased balance or
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secondary to the use of ambulatory assistive devices (Leroux et al., 2006). However, this
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group of authors did not use specific measures of balance. Previous studies have also
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shown that individuals with an ISCI have reduced balance during quasi-static stance
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performed with eyes open or eyes closed as revealed by an increase in the center of
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pressure (COP) mean velocity, sway area and root mean square distance compared to
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able-bodied individuals (Lemay et al., 2013). Moreover, individuals with SCI display a
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delayed onset of electromyographic activity in the ankle muscles following an external
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perturbation (Thigpen et al., 2009), which may further impair the ability to control
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balance.
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Duclos et al. developed a model to assess balance difficulty during functional tasks such
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as standing balance tasks (Duclos et al., 2012), walking on level surfaces (Duclos et al.,
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2009) and sitting pivot transfers (Gagnon et al., 2012). Using the kinematic and ground
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reaction force data collected in a laboratory environment, this model calculates the
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stabilizing and destabilizing forces – the theoretical forces necessary to stabilize or
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destabilize the person at each moment of the entire task (Duclos et al., 2009). This
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model assesses both the postural and dynamic components of balance during the
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performance of dynamic tasks when the base of support is moving and changing in
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shape or in size (Duclos et al., 2012) and thus provides a comprehensive understanding
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of balance difficulties. This model may therefore serve to optimize interventions in
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rehabilitation aimed at improving walking abilities and reducing the risk of falls among
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individuals with an ISCI.
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We thus conducted a comprehensive laboratory-based protocol to calculate the
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stabilizing/destabilizing forces to study balance during gait among individuals with an
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ISCI and their able-bodied counterparts. The main purpose of this study was to compare
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balance in these two groups during the single support phase of gait. This sub-phase of
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the gait cycle was chosen because weight bearing on one foot while progressing forward
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is a demanding and unstable subtask as previously shown in able-bodied and elderly
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individuals (Duclos et al., 2009, Duclos et al., 2012). Our specific objectives were as
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follows: (1) to compare the postural and dynamic components of balance in individuals
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with an ISCI and able-bodied participants during the single support phase of gait, as well
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as at specific moments during the single support phase; and (2) to identify
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biomechanical variables that explain the values of these forces. The main hypothesis
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was that compared to able-bodied individuals, both (postural and dynamic) components
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of balance are impaired in individuals with an ISCI. Since the equations used to calculate
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the stabilizing and destabilizing forces are based on recognized biomechanical factors
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related to balance such as the COM speed (Pai and Patton, 1997) and the distance
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between the COP and the limits of the base of support (Popovic et al., 2000), we
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expected these to be important explanatory factor of the maximal stabilizing force and
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the minimal destabilizing force respectively (Duclos et al., 2009, Duclos et al., 2012).
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Methods
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Participants
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A convenience sample of 17 individuals with a traumatic ISCI (AIS D) were recruited
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from both inpatients and outpatients of the SCI rehabilitation unit of the Institut de
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réadaptation Gingras-Lindsay-de-Montréal (IRGLM) and compared to 17 age-matched
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able-bodied controls. The inclusion criteria for the participants with an ISCI were: (1) the
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ability to stand for five minutes without external support and (2) the ability to walk
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independently for 15 m without ambulatory assistive devices. Participants were excluded
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if they presented other neurological deficits in addition to the SCI or if they had walking
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or balance difficulties prior to the SCI. None of the able-bodied participants reported
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having physical impairments that interfered with walking or balance. Ethical approval
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was obtained from the Research Ethics Committee of the Centre for Interdisciplinary
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Research in Rehabilitation of Greater Montreal (CRIR). Each participant provided written
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consent after having read and understood the information about the study. ***insert table 1 about here***
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Clinical assessment
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For the participants with an ISCI, demographic information regarding the date of injury
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and AIS level were gathered from the participant’s chart. An experienced physical
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therapist conducted the Lower Extremity Motor Score Assessment (LEMS) according to
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American Spinal Cord Injury Association (ASIA) standards (Kirshblum et al., 2011). The
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LEMS is an evaluation of lower extremity muscle strength of 5 major muscle groups,
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representing the myotome from L2 to S1, using a 6 point (0 to 5) ordinal scale. Natural
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walking speed was tested over a distance of 15 meters (Lam et al., 2008). Participants
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were asked to perform three trials at their self-selected comfortable walking speed
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without any walking assistive devices. Performance over the middle 10-m section was
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timed and speed was calculated (10-m divided by the time in second). The three trials
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were averaged and the mean walking speed was calculated.
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Gait assessment
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Kinematic and kinetic data for all participants were collected during a 3-hour assessment
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session conducted at the Pathokinesiology Laboratory at the IRGLM. Thirty-six skin-
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fixed infrared light emitting diodes (LEDs) were used to define the head, trunk, and
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bilateral upper and lower extremity segments. In addition, a six-marker probe was used
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to digitize the location of 13 bony landmarks to locate joint axes and to define the base
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of support (BOS). A system linking four synchronized motion analysis camera bars
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(Optotrak model 3020; Northern Digital Inc., Waterloo, Ontario, Canada) captured the
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three-dimensional (3D) coordinates of the markers at a sampling frequency of 60 Hz.
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Kinematic data were filtered with a fourth-order Butterworth zero-lag filter, with a cut-off
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frequency of 6 Hz. Anthropometric measurements of the trunk, head, lower and upper
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extremities were taken at the end of the laboratory session. These data were entered in
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the biomechanical calculation using the 3D link model segment (Winter et al., 1990). In
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terms of the kinetic data, three AMTI® force platforms, sequentially embedded in a 9-m
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long walkway, recorded the ground reaction forces at a frequency of 600 Hz. The data
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were filtered with a fourth-order Butterworth zero-lag filter, with a cut-off frequency of
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10 Hz and down-sampled to 60 Hz to match the kinematic data.
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Participants walked along the laboratory pathway at their self-selected comfortable
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speed. After a period of familiarization, five trials for each foot were recorded. Trials were
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analyzed for the lower extremity while stepping onto the force plate, between toe off and
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the following heel strike of the contralateral lower extremity.
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Data and statistical analyses
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Analyses were performed on the single support phase of the weakest lower extremity
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(right/left: 8/9 consecutive steps; based on the LEMS) for individuals with an ISCI to
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better reveal balance difficulties. For the able-bodied participants, balance parameters of
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eight right and nine left consecutive steps (i.e., single support phase only) were analyzed
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to match the data of the individuals with an ISCI.
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The single support phase of the gait cycle, from contralateral toe off to contralateral heel
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strike, was normalized from 1 to 100 (100 data points). Data were then analyzed using
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the stabilizing/destabilizing forces model. The stabilizing force (SF) is the theoretical
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force necessary to stop both the COP and the COM at the limit of the potential base of
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support (defined as the outside perimeter of the vertical projection of both feet on the
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floor) at each moment of the task. It is calculated with the following equation: = −
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∙ ∙ 2
where corresponds to the stabilizing force, to the participant’s mass, to to the horizontal distance between the position of the linear velocity of the COM and
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the COP and the limit of the base of support in the direction of the COM linear velocity
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(Duclos et al., 2009, Duclos et al., 2012). High stabilizing force values indicate higher
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levels of difficulty in controlling the velocity of the centre of mass. The destabilizing force
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(DF) is the force needed to move the COP to the limit of the base of support and is
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calculated with the following equation: ∙ = ℎ
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where corresponds to the destabilizing force, to the ground reaction force, to the
unitary vector normal to the contact surface, ℎ to the height of the COM from the to the horizontal distance between the position of the COP supporting surface and
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and the limit of the base of support in the direction of the COM linear velocity (Duclos et
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al., 2009, Duclos et al., 2012). Low destabilizing force values indicate a position of the
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body that is destabilized more easily. Mean stabilizing force and destabilizing force
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values over the single support phase, as well as the maximum stabilizing force value
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and the minimum destabilizing force value were averaged for each participant and used
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to characterize balance during the single support phase (Duclos et al., 2009). Mean
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values characterize overall stability during the single support phase while extreme
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values represent the maximal instability experienced during the task.
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Descriptive statistics (mean and SD) were calculated for the participants’ characteristics
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(e.g., age, height, mass, BMI, and time post lesion) and for the clinical assessments
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(e.g., natural walking speed, unipodal stance phase, and LEMS). For both groups of
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participants, the normality of the data distribution and the homogeneity of variance were
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explored using the Shapiro-Wilk test and Levene’s test, respectively. The maximal
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stabilizing force and the minimal destabilizing force of individuals with SCI and the COM
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speed at maximal destabilizing force of able-bodied participants were abnormally
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distributed. Logarithmic transformation was applied and successfully corrected the initial
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departure from normality (Field, 2009). Between-group differences for all balance
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difficulty parameters were explored using independent Student t-tests. To further
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appreciate the importance of group differences of the various parameters, Cohen’s d
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effect sizes were also computed (Cohen, 1988). The effect sizes were considered small
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(