Abstract
Background:
The biomechanical mechanisms underlying stair climbing limitations are poorly understood in people with multiple sclerosis (MS).
Research Questions:
Are trunk and pelvis motion and lower extremity joint moments during step ascent different between MS and control groups? Are step ascent biomechanics and stair climbing performance associated in people with MS?
Methods:
20 people with MS (49±12 years, EDSS range: 1.5-5.5) and ten control participants (48±12 years) underwent three-dimensional motion analysis while ascending a 15.2-cm step and also completed a timed Functional Stair Test. Main effects of group (MS vs Control) and limb (Stronger/Dominant vs Weaker/Non-dominant) and interactions were assessed using two-way analyses of variance. Associations between movement patterns during the step ascent and Functional Stair Test performance were performed using Pearson’s correlations and backward stepwise linear regression.
Results:
Significant group main effects were observed in greater sagittal pelvis excursion (p<0.001), greater sagittal (p=0.013) and frontal (p=0.001) trunk excursion, and lower trail limb peak ankle plantar flexion moment (p<0.001) of the MS group. Significant limb main effects were observed with greater sagittal trunk excursion (p=0.037) and peak trail limb ankle plantar flexion moment (p=0.037) in the stronger/dominant limb. A significant interaction was observed in peak knee extensor moment (p=.002). Stair climbing performance in the MS group correlated with sagittal (r=.607, p=<0.001) and frontal pelvis excursions (r=0.385, p=0.014), sagittal trunk excursion (r=.411, p=0.008), and ankle plantar flexion moments (r=−0.415, p=0.008). Sagittal and frontal pelvis excursion and bilateral handrail use explained a significant amount of variability in stair climbing performance (Adj R2=0.775).
Significance:
In conclusion, despite the presence of proximal and distal lower extremity movement pattern compensations during a step ascent task, larger pelvis angular excursions are associated with impaired stair climbing performance in people with MS and may serve as targets for future rehabilitation interventions.
Keywords: biomechanics, stair, multiple sclerosis, kinetic, moment
INTRODUCTION
Multiple sclerosis (MS) is a chronic autoimmune-mediated disorder of the central nervous system affecting nearly 1 million people in the United States [1]. Impaired functional mobility is a frequent problem and a contributor to decreased quality of life and reduced physical activity for people with MS [2-4]. Overground walking is the most studied functional mobility task in this population, with numerous studies reporting kinematic asymmetries and reduced lower-limb joint moments in people with MS compared to healthy age-matched control groups [5-7]. Compensations during walking are associated with relevant clinical measures such as trunk and lower extremity muscle strength and walking capacity [6-11]. While prior studies have informed rehabilitation interventions to improve walking in people with MS, there is limited evidence on higher-demand functional mobility tasks. Specifically, stair climbing, a critical functional mobility task for independence and community participation, is understudied in people with MS [12-14]. In order to more completely understand functional mobility limitations in people with MS, movement patterns involved with functional mobility tasks, such as stair climbing, must be systematically evaluated.
Stair climbing has unique task demands as it requires larger lower extremity joint moments and joint displacements, distinctive muscle coordination patterns, and places additional challenges on balance compared to walking [15, 16]. Corporaal et al. found greater sagittal trunk sway during stair navigation to be correlated with greater severity of disability in people with MS, as measured by the Expanded Disability Status Scale (EDSS). Carpinella et al. determined greater sagittal and frontal trunk sway during stair ascent correlated with lower gait and stair ascent ability as measured using the modified Dynamic Gait Index. These two previous studies utilized a single inertial measurement unit (IMU) to quantify trunk motion, which was limited to assessment of single-segment kinematics. Conversely, image-based motion capture with synced force platforms allows for more comprehensive kinematic and kinetic evaluation of human motion which can provide additional insight into the movement compensation strategies utilized for functional mobility tasks [7].
In addition to quantitatively evaluating movement compensations during a step ascent task, it is important to evaluate the relationship to relevant clinical measures such as stair climbing performance. Stair climbing ability is a crucial component of functional independence and quality of life in people with neurological conditions [13, 17]. The Functional Stair Test is a reliable test used for clinical assessment of stair navigation [14], however, knowledge of the relationships between movement compensations during a step ascent task and the Functional Stair Test has not been reported and may be overlooked as targets for rehabilitation intervention. Therefore, image-based motion analysis of a step ascent task and evaluation of the relationships between movement compensation and stair climbing performance would inform clinical rehabilitation approaches.
The aim of the current study was to: 1) compare trunk and pelvis motion and lower extremity joint moments during a step ascent task in people with MS and an age-and-sex comparable control group and 2) identify associations between biomechanical variables of a step ascent task and stair ascent performance in people with MS. Based on the evidence cited above, we hypothesized people with MS would complete a step ascent task with greater trunk and pelvis motion and reduced lower extremity joint moments 1) in the weaker limb compared to the stronger limb and 2) compared to the control group. Finally, we hypothesized greater trunk and pelvis motion during the step ascent task would correlate with poorer stair ascent performance in people with MS.
METHODS
Participants and Study Setting
Two groups were evaluated in this cross-sectional study, people with MS (n=20) and age-and-sex comparable healthy participants (n=10). MS group inclusion criteria: neurologist-confirmed MS diagnosis, 18-65 years old, and an EDSS <6. MS group exclusion criteria: neurologist-confirmed MS exacerbation within the past month, drug therapy change within the past month, or greater than minimal spasticity (Modified Ashworth Scale ≥ 2) [18]. Control group inclusion criteria: no neurologic or musculoskeletal pathologies and matched the sex (male or female) and mean age (within ±3 years) of two MS participants. Control group exclusion criteria: pain limiting ambulation or inability to ambulate 100 meters without an assistive device. All participants signed informed consent documents approved by the Colorado Multiple Institutional Review Board. All testing occurred in a university-based human performance laboratory.
Descriptive Measures
The EDSS, performed by a licensed physical therapist trained in EDSS administration, was used to classify the level of disability and identify the stronger lower limb in the MS group. Potential EDSS scores range from 0 (no disability) to 10 (death due to MS), with scores <6 indicating the ability to walk at least 100 meters without aid or rest [19]. Other descriptive measures included age, body height and mass, and sex for both groups.
Three-dimensional Motion Analysis
All participants underwent three-dimensional video motion analysis while ascending a 15.2 cm step using a passive marker set of 63 markers placed on the head (5 markers), trunk (7 markers), pelvis (9 markers), and bilateral upper (6 markers each) and lower extremities (15 markers each) [20]. Participants began by standing shod in front of the step and were instructed to ascend and come to rest at the top of the step. A familiarization trial was allowed for each limb to ensure safe performance without supervision or use of upper extremity support. Following familiarization, three trials were recorded with each limb as the leading limb. Balance poles were available to participants prior to initiating the step ascent, but were not used during step task performance. Marker trajectories were recorded using an 8-camera motion analysis system (Vicon Motion Systems, Oxford, UK) with a sampling rate of 100 Hz. Two force platforms, one in front of the step where the participant initiated the step ascent and one directly underneath the step, simultaneously recorded force data at 1200 Hz (Bertec, Columbus, OH, USA).
Stair Climbing Performance
Stair climbing performance was assessed using the ascent time of the Functional Stair Test, a reliable test in people with MS [14]. Participants were timed using a hand-held stopwatch as they ascended one flight of 4 steps (each 23.5x76.2x15.2 cm) as quickly and safely as possible with handrail use allowed as needed. Two trials were performed with each recorded to the nearest 0.01 second and the mean of both trials was used for data analysis.
Data Reduction & Statistical Analysis
Visual3D software (C-Motion, Inc. Germantown, MD, USA) was used to filter the data, calculate joint kinematics, and calculate joint moments during the step ascent task. Marker position and force data were filtered at 6 and 20 Hz, respectively (fourth-order, low-pass, zero-lag Butterworth filter). Lower extremity joint moments were calculated using Cardan XYZ angles referencing the distal segment to the proximal and were normalized to body mass. Custom MATLAB (MathWorks, Natick, MA, USA) code was used to extract lower-limb joint moments and pelvis and trunk kinematics from the instant the lead limb contacted the step until the trail limb contacted the step. Peak hip, knee, and ankle moments were averaged from the three step ascent trials. Total trunk and pelvis angular excursions (sagittal and frontal) were determined as the difference between minimum and maximum segment angle.
Continuous variables were described using mean and standard deviation. Categorical variables (e.g., sex) were tabulated with absolute frequency. Data were checked for normality using Shapiro-Wilk tests. The dominant limb for the control group was determined by asking which limb they would use to kick a ball. Main effects of group (MS vs Control) and limb (Stronger/Dominant vs Weaker/Non-dominant) and group*limb interactions were assessed using a 2-way analysis of variance. Correlations between movement patterns during the step ascent task and stair climbing performance of the MS group were performed using Pearson product moment correlations.
Backward stepwise linear regression was used to explore the primary biomechanical variables associated with stair climbing performance in the MS group. Biomechanical variables with Pearson correlation significance levels of p<0.1 were eligible for inclusion in the regression model. Rail use (1 or 0 rails used; 2 rails used) during the Functional Stair Test was included as a covariate in the regression model as a proxy for balance or limb muscle impairment. In each step, the predictor variable with the highest p-value >0.1 was excluded until the final model included only significant variables (p<0.05). Multicollinearity was assessed using variance inflation factors with a value >5 indicating the presence of multicollinearity. All statistical tests were performed using SPSS Statistics 26 (IBM, Armonk, NY, USA) with statistical significance defined as p <0.05. Using previously published data for sagittal plane trunk sway during stair ascent in people with MS compared to a control group [12], an a-priori sample size calculation conservatively assuming an effect size d of 1.7, α = 0.05, and 90% power to detect differences between MS and control group participants recommended a total sample of 10 participants per group (G*Power, Dusseldorf, Germany). To account for additional correlation and regression analyses, the total sample size of the MS group was increased to 20 participants.
RESULTS
Twenty-one people were enrolled in the MS group along with 10 control group participants. Data from one participant with MS was excluded from analysis due to technical issues during data collection. There were no between-group differences in age and sex (Table 1). The control group Functional Stair Test time was significantly faster than the MS group (p<.001). Two MS group participants did not use handrails during either Functional Stair Test trial, 10 used a single rail, and eight used bilateral handrails.
Table 1.
Demographic and stair climbing performance comparisons between the MS and CTL groups.
| Measure | MS (n=20) | CTL (n=10) | p-value |
|---|---|---|---|
| Age (years) | 49 ± 12 | 48 ± 12 | 0.859 |
| Sex (Female, %) | 16 (80%) | 7 (70%) | 0.105 |
| Body Mass Index (kg/m2) | 24.8 ± 5.4 | 23.7 ± 4.2 | 0.577 |
| EDSS (median, range) | 3.5 (1.5 – 5.5) | - | - |
| Functional Stair Test Time (seconds) | 3.45 ± 0.75 | 1.66 ± 0.22 | <0.001* |
All measures presented as mean ± SD unless otherwise noted.
MS: Multiple sclerosis, CTL: control, EDSS: Expanded Disability Status Scale
All biomechanical outcomes were normally distributed. Significant between-group main effects were observed in greater sagittal pelvis excursion (p<0.001), greater sagittal (p=0.013) and frontal (p=0.001) trunk excursion, and lower peak ankle plantar flexion moment in the trail limb (p<0.001) of the MS group. Significant between-limb main effects were observed when leading step ascent with the stronger/dominant limb, with greater sagittal trunk excursion (p=0.037) and peak ankle plantar flexion moment in the trail limb (p=0.037) in the stronger/dominant limb. A significant interaction was observed in peak knee extensor moment (p=.002) with the MS group demonstrating greater between-limb asymmetry than the control group (Table 2).
Table 2:
Analysis of Variance results for angular excursions and joint moments during step ascent task.
| MS Stronger | MS Weaker | CTL Dominant |
CTL Non- Dominant |
Group Main Effect p-value |
Limb Main Effect p-value |
Group*Limb Interaction p-value |
|
|---|---|---|---|---|---|---|---|
| Pelvis Excursion-Sagittal (°) | 10.4 ± 4.0 | 10.1 ± 5.2 | 5.8 ± 1.7 | 5.0 ± 2.7 | <0.001* | 0.667 | 0.826 |
| Pelvis Excursion-Frontal (°) | 6.3 ± 3.3 | 6.1 ± 3.1 | 7.7 ± 1.9 | 7.1 ± 1.0 | 0.119 | 0.593 | 0.780 |
| Trunk Excursion-Sagittal (°) | 9.3 ± 3.1 | 7.6 ± 2.6 | 7.3 ± 2.9 | 5.7 ± 2.6 | 0.013* | 0.037* | 0.975 |
| Trunk Excursion-Frontal (°) | 5.1 ± 2.2 | 5.2 ± 2.6 | 3.2 ± 1.7 | 3.1 ± 1.5 | 0.001* | 0.992 | 0.860 |
| Peak Hip Ext Moment (Nm/kg) | 0.49 ± 0.20 | 0.52 ± 0.25 | 0.51 ± 0.18 | 0.48 ± 0.22 | 0.899 | 0.960 | 0.584 |
| Peak Knee Ext Moment (Nm/kg) | 1.19 ± 0.29 | 0.88 ± 0.23 | 1.04 ± 0.15 | 1.14 ± 0.10 | 0.402 | 0.080 | 0.002* |
| Peak PF Moment - Lead (Nm/kg) | 0.52 ± 0.19 | 0.45 ± 0.15 | 0.53 ± 0.18 | 0.55 ± 0.19 | 0.256 | 0.670 | 0.389 |
| Peak PF Moment -Trail (Nm/kg) | 1.11 ± 0.17† | 0.92 ± 0.24# | 1.28 ± 0.20 | 1.24 ± 0.15 | <0.001* | 0.037* | 0.173 |
Sagittal and frontal pelvis angular excursions, sagittal trunk excursion, and trail limb peak ankle plantar flexion moments were correlated with Functional Stair Test performance in people with MS (Table 3; Figure 1). Greater pelvis and trunk excursions and lower trail limb ankle plantar flexion moments were independently associated with slower stair ascent times. No additional significant correlations were observed. Five biomechanical variables qualified for inclusion into the backward regression model based on correlation analyses: sagittal and frontal pelvis excursion, sagittal and frontal trunk excursion, and peak plantar flexion moment of the trail limb. In addition to bilateral handrail use (p<0.001), the final regression model included only sagittal (p=0.019) and frontal (p<0.001) pelvis excursion as significant predictors of stair ascent time in people with MS (Adj R2 = 0.775) (Table 4). Multicollinearity was not observed between the final predictor variables (VIF= 1.012-1.462).
Table 3.
Correlations of step ascent biomechanical variables to stair climbing performance.
| Stair Ascent Time (s) | |
|---|---|
| Pelvis Excursion-Sagittal (°) | 0.607* (p<0.001) |
| Pelvis Excursion-Frontal (°) | 0.385* (p=0.014) |
| Trunk Excursion-Sagittal (°) | 0.411* (p=0.008) |
| Trunk Excursion-Frontal (°) | −0.291 (p=0.069) |
| Peak Hip Ext Moment (Nm/kg) | −0.031 (p=0.851) |
| Peak Knee Ext Moment (Nm/kg) | −0.063 (p=0.700) |
| Peak PF Moment – Lead (Nm/kg) | 0.148 (p=0.363) |
| Peak PF Moment – Trail (Nm/kg) | −0.415* (p=0.008) |
Ext: extension
PF: plantar flexion
statistically significant (Alpha < 0.05)
Figure 1.
Scatterplots of correlations between stair climbing performance and A) sagittal plane pelvis excursion, B) frontal plane pelvis excursion, C) sagittal plane trunk excursion, and D) peak ankle plantar flexion moment of the stronger and weaker limbs of the MS group during step ascent. Participant handrail use is identified as ▴ = no rail used, ●= 1 rail used, X = bilateral rails used.
Table 4:
Results of regression model predicting stair climbing performance.
| Candidate variable | B (95% CI) | Standard Error | VIF | P-value |
|---|---|---|---|---|
| Final Model | ||||
| Pelvis Excursion - Sagittal | 0.036 (0.006, 0.066) | 0.015 | 1.426 | 0.019 * |
| Pelvis Excursion - Frontal | 0.070 (0.033, 0.106) | 0.018 | 1.012 | <0.001 * |
| Handrail Use | 0.991 (0.715, 1.267) | 0.136 | 1.435 | <0.001 * |
| Constant | 2.245 (1.890, 2.601) | 0.175 | - | - |
| Excluded Variables | ||||
| Trunk Excursion – Sagittal | 0.003 (−0.048, 0.053) | 0.025 | 1.571 | 0.917 |
| Trunk Excursion – Frontal | −0.028 (−0.086, 0.030) | 0.029 | 1.478 | 0.334 |
| Ankle PF Moment - Trail | −0.281 (−0.894, 0.332) | 0.302 | 1.456 | 0.358 |
B: unstandardized beta
CI: confidence interval
VIF: variance inflation factor
PF: plantar flexion
Trail: trail limb
statistically significant (Alpha < 0.05)
DISCUSSION
In line with our hypotheses, this study demonstrated that the MS group, compared to the control group, moved with greater sagittal pelvis excursion, greater sagittal and frontal trunk excursion, and lower peak plantar flexion moment of the trail limb when performing a step-up task. Significant main effects for stronger/dominant limb compared to the weaker/non-dominant limb were observed in sagittal trunk excursion and peak plantar flexion moment of the trail limb. In addition, a group*limb interaction was observed for peak knee extension moment. Greater pelvis angular excursions in the sagittal and frontal planes, greater trunk excursion in the sagittal plane, and lower trail limb peak ankle plantarflexion moments were significantly correlated with poorer stair climbing performance in people with MS. The regression model identified greater sagittal and frontal plane pelvis excursions as factors explaining a significant amount of variability in stair climbing performance in people with MS that could be modified with rehabilitation intervention.
Importantly, the results of this study complement and extend previous work indicating sagittal trunk angular excursion during step ascent as an indicator of function and dynamic balance in people with MS [10, 12]. We identified greater sagittal and frontal trunk angular excursion during the step ascent in the MS group compared to the control group and found greater sagittal trunk excursion correlates with slower Functional Stair Test time. In addition, our results extend previous work as we identified impairments in sagittal and frontal pelvis angular excursions as primary contributors to variability in stair climbing performance [10, 12].
Methodological differences between the current and prior studies may account for the result of pelvis angular excursion correlating to stair climbing ability, instead of trunk angular excursion. Two prior studies utilized a single IMU to quantify trunk motion without consideration of trunk motion relative to the pelvis [10, 12]. In contrast, our model quantified pelvis motion relative to the global coordinate system and reported trunk motion relative to the pelvis. Thus, it may be that pelvis angular excursion contributed to some amount of the trunk motion observed in the prior studies. These methodological differences may increase measurement sensitivity compared to using a global coordinate system and account for the significant between-group differences and correlations we observed in frontal trunk angular excursion. Nevertheless, the current results suggest proximal (i.e., pelvis and trunk) control and stability to be a critical factor in successful stair navigation.
Between-group and between-limb differences indicate reduced peak plantar flexion moment of the trail limb in the MS group and in the weaker/non-dominant limb. In addition, group*limb interactions in peak knee extensor moment suggest asymmetries in knee extensor moment of the lead limb were larger in the MS group than the control group. To our knowledge, this is the first study to report lower extremity joint kinetics during a step ascent task in people with MS. The findings support prior work in overground walking which identified reduced peak ankle plantar flexion moments in the trail limb and reduced knee extension moment in the lead limb in people with MS [7]. Reduced plantar flexion moments limit forward progression and swing initiation during overground walking and may limit upward progression of the individual’s center of mass during step ascent [15, 21]. Further, step ascent places approximately twice the demand on the knee extensor muscles as overground level walking [15], and knee extensor muscle weakness is a common impairment in people with MS [9, 22]. The greater trunk and pelvis motion observed during stair ascent may be a strategy to compensate for knee extension muscle weakness with reduced knee moment [23]. However, trunk and hip muscle weakness are also common in people with MS and are strong contributors to functional mobility [11, 24]. The results of the regression model suggest pelvis angular excursion explains more variance in stair climbing performance than peak knee or ankle joint moments even when accounting for handrail use. As such, sufficient proximal motor control, stability, and/or muscle strength (e.g., hip abductors, trunk) may be critical for stair climbing ability and impairments in these areas may contribute to the observed proximal movement compensations.
Prior study of step ascent biomechanics in people with MS is limited. However, several studies have evaluated improvement in stair climbing performance using exercise-based interventions. Separate randomized control trials demonstrated improvement in stair climbing performance following 12 and 24-week progressive lower extremity resistance training [25, 26]. Conversely, Hayes et al. reported high-intensity eccentric lower extremity strength training did not improve stair climbing performance compared to a general exercise program of aerobic training, stretching, resistance training, and balance activities [27]. Of interest, only the group participating in the general exercise program demonstrated improved stair climbing performance [27]. Tarakci et al. observed an improvement in stair climbing ability following a 12-week program of functional training, core strengthening, balance training, and lower extremity resistance exercise [28]. The results of Hayes et al. and Tarakci et al. suggest that resistance training alone may have limited benefits for stair climbing performance. Rather, activities emphasizing balance and motor control may be more effective. To this point, better dynamic balance is associated with improved stair climbing ability [10, 12], therefore, the balance training activities in these prior studies may have contributed to improved proximal control, potentially facilitating improved stair climbing performance.
Excessive trunk motion during step ascent is also documented in other patient populations with known balance impairments including people with lower limb amputation, mild traumatic brain injury, and unilateral vestibular deficits [20, 29, 30]. Although dynamic balance was not quantitatively evaluated in the current study, bilateral handrail use during the Functional Stair Test was used as a proxy for balance and limb weakness and its statistical significance in the final regression model supports prior evidence of balance impairments limiting stair function. Prior evidence, in combination with the current study, suggest improving proximal strength and coordination through exercise and balance training may limit excessive pelvis angular excursion and improve stair climbing performance.
Limitations.
The cross-sectional design precludes determining causality between biomechanics and stair climbing performance. Although adequately powered for the primary analyses, the relatively small sample size may have limited the ability to detect significant group*limb interactions. Although handrail use was statistically accounted for, this study did not assess underlying reasons for handrail use such as muscle strength, postural stability, or motor coordination and their relationship to biomechanics or stair climbing performance. In addition, the step ascent task simulates stair climbing with a step-to pattern which may not represent a step-over-step pattern when ascending a full flight of stairs. Lastly, including strength, quantitative postural stability metrics, and motor coordination assessments in a larger sample would allow for analysis of contributions to step up performance from multiple domains.
CONCLUSIONS
In conclusion, despite proximal and distal lower extremity movement pattern compensations during a step ascent task, larger pelvis angular excursions are associated with worse stair climbing performance in people with MS and may serve as targets for future rehabilitation interventions.
ACKNOWLEDGEMENTS
The authors would like to acknowledge Meg O’Connor and Nicola Haakonsen for their assistance with data processing and participant recruitment. This work was supported by a grant from the Department of Physical Medicine and Rehabilitation at the University of Colorado Anschutz Medical Campus and the Colorado Clinical & Translational Science Institute (NIH/NCATS UL1-TR001082, TL1-TR002535). The funding sources had no role in the design, execution, analysis, interpretation of the data, writing of the article, or decision to submit the article for publication. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH, the U.S. Department of Veterans Affairs, or the United States Government.
Footnotes
DECLARATIONS OF INTEREST
None
REFERENCES
- [1].Wallin MT, Culpepper WJ, Campbell JD, Nelson LM, Langer-Gould A, Marrie RA, Cutter GR, Kaye WE, Wagner L, Tremlett H, Buka SL, Dilokthornsakul P, Topol B, Chen LH and LaRocca NG, The prevalence of ms in the united states: A population-based estimate using health claims data, Neurology. 92 (2019) e1029–e1040. 10.1212/wnl.0000000000007035 [DOI] [PMC free article] [PubMed] [Google Scholar]
- [2].Stevens V, Goodman K, Rough K and Kraft GH, Gait impairment and optimizing mobility in multiple sclerosis, Phys Med Rehabil Clin N Am. 24 (2013) 573–92. 10.1016/j.pmr.2013.07.002 [DOI] [PubMed] [Google Scholar]
- [3].Zwibel HL, Contribution of impaired mobility and general symptoms to the burden of multiple sclerosis, Adv Ther. 26 (2009) 1043–57. 10.1007/s12325-009-0082-x [DOI] [PubMed] [Google Scholar]
- [4].Backus D, Increasing physical activity and participation in people with multiple sclerosis: A review, Arch Phys Med Rehabil. 97 (2016) S210–7. 10.1016/j.apmr.2015.09.027 [DOI] [PubMed] [Google Scholar]
- [5].Comber L, Galvin R and Coote S, Gait deficits in people with multiple sclerosis: A systematic review and meta-analysis, Gait Posture. 51 (2017) 25–35. 10.1016/j.gaitpost.2016.09.026 [DOI] [PubMed] [Google Scholar]
- [6].Spain RI, St George RJ, Salarian A, Mancini M, Wagner JM, Horak FB and Bourdette D, Body-worn motion sensors detect balance and gait deficits in people with multiple sclerosis who have normal walking speed, Gait Posture. 35 (2012) 573–8. 10.1016/j.gaitpost.2011.11.026 [DOI] [PMC free article] [PubMed] [Google Scholar]
- [7].Huisinga JM, Schmid KK, Filipi ML and Stergiou N, Gait mechanics are different between healthy controls and patients with multiple sclerosis, J Appl Biomech. 29 (2013) 303–11. 10.1123/jab.29.3.303 [DOI] [PubMed] [Google Scholar]
- [8].Verheyden G, Nuyens G, Nieuwboer A, Van Asch P, Ketelaer P and De Weerdt W, Reliability and validity of trunk assessment for people with multiple sclerosis, Phys Ther. 86 (2006) 66–76. 10.1093/ptj/86.1.66 [DOI] [PubMed] [Google Scholar]
- [9].Thoumie P, Lamotte D, Cantalloube S, Faucher M and Amarenco G, Motor determinants of gait in 100 ambulatory patients with multiple sclerosis, Mult Scler. 11 (2005) 485–91. 10.1191/1352458505ms1176oa [DOI] [PubMed] [Google Scholar]
- [10].Corporaal SH, Gensicke H, Kuhle J, Kappos L, Allum JH and Yaldizli O, Balance control in multiple sclerosis: Correlations of trunk sway during stance and gait tests with disease severity, Gait Posture. 37 (2013) 55–60. 10.1016/j.gaitpost.2012.05.025 [DOI] [PubMed] [Google Scholar]
- [11].Manago MM, Kline PW, Alvarez E and Christiansen CL, Trunk and pelvis movement compensation in people with multiple sclerosis: Relationships to muscle function and gait performance outcomes, Gait Posture. 78 (2020) 48–53. 10.1016/j.gaitpost.2020.03.006 [DOI] [PubMed] [Google Scholar]
- [12].Carpinella I, Gervasoni E, Anastasi D, Lencioni T, Cattaneo D and Ferrarin M, Instrumental assessment of stair ascent in people with multiple sclerosis, stroke, and parkinson's disease: A wearable-sensor-based approach, IEEE Trans Neural Syst Rehabil Eng. 26 (2018) 2324–2332. 10.1109/tnsre.2018.2881324 [DOI] [PubMed] [Google Scholar]
- [13].Alzahrani MA, Dean CM and Ada L, Ability to negotiate stairs predicts free-living physical activity in community-dwelling people with stroke: An observational study, Aust J Physiother. 55 (2009) 277–81. 10.1016/s0004-9514(09)70008-x [DOI] [PubMed] [Google Scholar]
- [14].Fry DK and Pfalzer LA, Reliability of four functional tests and rating of perceived exertion in persons with multiple sclerosis., Physiotherapy Canada. 58 (2006) 212–220. [Google Scholar]
- [15].Nadeau S, McFadyen BJ and Malouin F, Frontal and sagittal plane analyses of the stair climbing task in healthy adults aged over 40 years: What are the challenges compared to level walking?, Clin Biomech (Bristol, Avon). 18 (2003) 950–9. 10.1016/s0268-0033(03)00179-7 [DOI] [PubMed] [Google Scholar]
- [16].Conway ZJ, Silburn PA, Blackmore T and Cole MH, Evidence of compensatory joint kinetics during stair ascent and descent in parkinson's disease, Gait Posture. 52 (2017) 33–39. 10.1016/j.gaitpost.2016.11.017 [DOI] [PubMed] [Google Scholar]
- [17].van Iersel MB, Olde Rikkert MG and Mulley GP, Is stair negotiation measured appropriately in functional assessment scales?, Clin Rehabil. 17 (2003) 325–33. 10.1191/0269215502cr628oa [DOI] [PubMed] [Google Scholar]
- [18].Bohannon RW and Smith MB, Interrater reliability of a modified ashworth scale of muscle spasticity, Phys Ther. 67 (1987) 206–7. 10.1093/ptj/67.2.206 [DOI] [PubMed] [Google Scholar]
- [19].Kurtzke JF, Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (edss), Neurology. 33 (1983) 1444–52. 10.1212/wnl.33.11.1444 [DOI] [PubMed] [Google Scholar]
- [20].Murray AM, Gaffney BM, Davidson BS and Christiansen CL, Biomechanical compensations of the trunk and lower extremities during stepping tasks after unilateral transtibial amputation, Clin Biomech (Bristol, Avon). 49 (2017) 64–71. 10.1016/j.clinbiomech.2017.08.010 [DOI] [PMC free article] [PubMed] [Google Scholar]
- [21].McFadyen BJ and Winter DA, An integrated biomechanical analysis of normal stair ascent and descent, J Biomech. 21 (1988) 733–44. 10.1016/0021-9290(88)90282-5 [DOI] [PubMed] [Google Scholar]
- [22].Guner S, Haghari S, Inanici F, Alsancak S and Aytekin G, Knee muscle strength in multiple sclerosis: Relationship with gait characteristics, J Phys Ther Sci. 27 (2015) 809–13. 10.1589/jpts.27.809 [DOI] [PMC free article] [PubMed] [Google Scholar]
- [23].Asay JL, Mundermann A and Andriacchi TP, Adaptive patterns of movement during stair climbing in patients with knee osteoarthritis, J Orthop Res. 27 (2009) 325–9. 10.1002/jor.20751 [DOI] [PubMed] [Google Scholar]
- [24].Manago MM, Hebert JR, Kittelson J and Schenkman M, Contributions of ankle, knee, hip, and trunk muscle function to gait performance in people with multiple sclerosis: A cross-sectional analysis, Phys Ther. 98 (2018) 595–604. 10.1093/ptj/pzy048 [DOI] [PubMed] [Google Scholar]
- [25].Kjolhede T, Vissing K, de Place L, Pedersen BG, Ringgaard S, Stenager E, Petersen T and Dalgas U, Neuromuscular adaptations to long-term progressive resistance training translates to improved functional capacity for people with multiple sclerosis and is maintained at follow-up, Mult Scler. 21 (2015) 599–611. 10.1177/1352458514549402 [DOI] [PubMed] [Google Scholar]
- [26].Dalgas U, Stenager E, Jakobsen J, Petersen T, Hansen HJ, Knudsen C, Overgaard K and Ingemann-Hansen T, Resistance training improves muscle strength and functional capacity in multiple sclerosis, Neurology. 73 (2009) 1478–84. 10.1212/WNL.0b013e3181bf98b4 [DOI] [PubMed] [Google Scholar]
- [27].Hayes HA, Gappmaier E and LaStayo PC, Effects of high-intensity resistance training on strength, mobility, balance, and fatigue in individuals with multiple sclerosis: A randomized controlled trial, J Neurol Phys Ther. 35 (2011) 2–10. 10.1097/NPT.0b013e31820b5a9d [DOI] [PubMed] [Google Scholar]
- [28].Tarakci E, Yeldan I, Huseyinsinoglu BE, Zenginler Y and Eraksoy M, Group exercise training for balance, functional status, spasticity, fatigue and quality of life in multiple sclerosis: A randomized controlled trial, Clin Rehabil. 27 (2013) 813–22. 10.1177/0269215513481047 [DOI] [PubMed] [Google Scholar]
- [29].Findling O, Schuster C, Sellner J, Ettlin T and Allum JH, Trunk sway in patients with and without, mild traumatic brain injury after whiplash injury, Gait Posture. 34 (2011) 473–8. 10.1016/j.gaitpost.2011.06.021 [DOI] [PubMed] [Google Scholar]
- [30].Allum JH, Adkin AL, Carpenter MG, Held-Ziolkowska M, Honegger F and Pierchala K, Trunk sway measures of postural stability during clinical balance tests: Effects of a unilateral vestibular deficit, Gait Posture. 14 (2001) 227–37. 10.1016/s0966-6362(01)00132-1 [DOI] [PubMed] [Google Scholar]