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Table 2 Summary of the studies (n = 42) included on the review in the alphabetical order

From: Research on lower extremity health in patients with multiple sclerosis: a systematic scoping review

Author, year, country Aim Design, sample Data collection method Main results Quality appraisal
(number of fulfilled criteria)
Boes et al. 2018,
USA [45]
To determine whether a powered ankle-foot orthosis (AFO) that provides dorsiflexor and plantar flexor assistance at the ankle can improve walking endurance of persons with multiple sclerosis Short-term intervention;
n = 16 PwMS, mean age 54.6
Walking test Powered ankle-foot orthosis did not improve endurance walking performance. 4
Boudarham et al.
2016, Switzerland [46]
To assess coactivation of agonist and antagonist muscles at the knee and ankle joints during gait in patients with multiple sclerosis, and to evaluate the relationship between muscle coactivation and disability, gait performance, dynamic ankle strength measured during gait, and postural stability. Design not reported;
n = 14 PwMS, mean age 51
3D-gait analysis Coactivation was increased in the knee muscles during single support (proximal strategy) and in the ankle muscles during double support (distal strategy). The magnitude of coactivation was highest in the patients with the slowest gait, the greatest motor impairment and the most instability. 3
Bowser et al. 2015,
USA [47]
To compare sit-to-stand biomechanics among three groups: people with multiple sclerosis who exhibit leg weakness, people with multiple sclerosis who have comparable strength to controls, and healthy controls. Cross-sectional design;
n = 21 PwMS divided in two groups:
Leg weakness group n = 10, mean age 49.2
Comparable strength group n = 11, mean age 39.8
Lower extremity muscle strength Persons with multiple sclerosis exhibiting leg weakness displayed decreased leg strength, greater trunk flexion, faster trunk flexion velocity and decreased knee extensor power compared to the other two groups, and slower rise times compared to controls. 3
Brincks et al. 2017, Denmark [48] To examine the associations between postural balance, assessed by force platform stabilometry, and complex walking performance and maximal walking speed in mildly disabled persons with MS and healthy matched controls. Cross-sectional study design;
n = 13 PwMS, mean age 42
Walking performance, postural balance Significant correlations were observed between sway area and Timed Up & Go and fastest safe walking speed in persons with MS. 4
Broekmans et al.
2010,
Belgium [49]
To investigate the acute effects of long-term wholebody vibration on leg muscle performance and functional capacity in persons with multiple sclerosis. A randomized controlled trial;
n = 25 PwMS, mean age 47.9
Muscle maximal isometric and dynamic strength, strength endurance and speed of movement, function. Leg muscle performance and functional capacity were not altered following 10 or 20 weeks of whole-body vibration. 4
Citaker et al. 2011,
Turkey [50]
To investigate the relationship between the foot sensations and standing balance in patients with Multiple Sclerosis (MS) and find out the sensation, which best predicts balance. Design not reported;
n = 27 PwMS, mean age 36.74
Sensation, vibration sensation, standing on one-leg Light touch-pressure, vibration, two-point discrimination sensations of the foot sole, and duration of one-leg standing balance were decreased in patients with MS. Sensation of the foot sole was related with duration of one-leg standing balance in patients with MS. 4
Citaker et al. 2013,
Turkey [51]
To investigate the relationship between the lower extremity isometric muscle strength and standing balance in patients with MS. Design not reported;
n = 47 PwMS, mean age 36.98
Neurological disability, muscle strength, static one-leg standing balance Hip flexor-extensor-abductor-adductor, knee flexor-extensor, and ankle dorsal flexor isometric muscle strength, and duration of one-leg standing balance were decreased in patients with MS. All assessed lower extremity isometric muscle strength and EDSS level were related duration of one-leg standing balance in patients with MS. All assessed lower extremity isometric muscle strength (except ankle dorsal flexor) was related with EDSS. 4
DeBolt et al. 2004,
USA [52]
To examine the effects of an 8-week home-based resistance exercise program on balance, power, and mobility in adults with multiple sclerosis. Pretest–posttest experimental group design;
n = 29 female PwMS, mean age 50.3
n = 8 male PwMS, mean age 51.1
divided into exercise group and control group
Balance, mobility, leg power Leg extensor power improved significantly in the exercise group, although measures of balance and mobility did not change. 4
Dodd et al. 2011,
Australia [53]
To determine the effectiveness of progressive resistance training (PRT) for people with MS, focusing on improving the gait deficits common in this population. Single blind randomized controlled trial; experimental group n = 36 PwMS, mean age 47.7
control group n = 35 PwMS, mean age 50.4
Walking endurance, maximal walking speed, muscle strength, muscle endurance, self-reported fatigue, health-related quality of life, muscle stiffness and spasm No differences were detected in walking performance. PRT demonstrated increased leg press strength, increased reverse leg press strength, and increased muscle endurance of the reverse leg press. 4
Fritz et al. 2015,
USA [54]
To determine the longitudinal relationships among quantitative measures of gait and balance in individuals with MS. Longitudinal cohort study;
n = 57 PwMS, mean age 45.86
Balance, walking, muscle strength, vibration Increases in static posturography and reductions in dynamic posturography are associated with a decline in walk velocity and Timed 25-Foot Walk performance over time. 4
Gutierrez et al. 2005,
USA [55]
To evaluate the effects of an 8-week lower-body resistance-training program on walking mechanics in persons with multiple sclerosis (MS) Repeated-measures design;
n = 8 PwMS, mean age 46.0
Kinematic gait parameters, isometric strength,3-min stepping, fatigue, self-reported disability Resistance training increased significantly percentage of stride time in the swing phase, step length, stride length, and foot angle; and significantly decreased percentage of stride time in the stance and double-support phases, duration of the double-support phase, and toe clearance. Isometric leg strength improved in 2 of the 4muscle groups tested. Fatigue indices decreased, whereas self-reported disability tended to decrease following the training program. 4
Hayes et al. 2011,
USA [18]
To assess the effects of a program of high-intensity RENEW exercise combined with standard exercises on lower extremity strength, mobility, balance, and fatigue in individuals with MS compared to a standard exercise program over 12 weeks. A prospective, longitudinal, randomized intervention trial;
n = 19 PwMS, mean age 49
Lower extremity strength, walking, balance, fatigue No significant time effects or interactions were observed for strength, walking or balance. 4
Huisinga et al. 2013,
USA [56]
To determine any differences in biomechanical gait parameters between patients with MS and healthy controls. Quantitative evaluation;
n = 31 PwMS, mean age 46.2
Joint torques and joint powers, walking Reduced angular range, less joint torque, and reduced joint power were seen in patients with MS. Significant correlations between biomechanical gait parameters and EDSS score. 4
Jackson et al. 2008,
USA [57]
To evaluate the acute effects of a brief exposure to WBV on quadriceps and hamstring muscle performance in persons with MS Randomized, crossover study;
n = 15 PwMS, mean age 54.6
Muscle torque There were no significant differences in isometric torque production between the 2- and 26-Hz WBV conditions. There was also no significant difference between baseline torque values and those measured at one, 10, and 20 min after either vibration exposure. 5
Kalron
2017a,
Israel [58]
To examine the relationship of obesity with walking and balance in people with multiple sclerosis. A cross-sectional study;
N = 436 PwMS divided into two groups:
n = 258 normal weight, mean age 40.4
n = 178 obese, mean age 49.6
Spatiotemporal parameters of gait, postural control Obese subjects walked significantly slower, with shorter step lengths and a wider step width. Thy walked a shorter distance on the 6-Minute Walk test and slower on the Timed 25-Foot Walk test. 5
Kalron
2017b,
Israel [59]
To examine the relationship between variability of major spatio-temporal parameters of gait and falls, in PwMS with an expanded disability status scale score of 4.0 and 4.5 Cross-sectional study;
N = 91 PwMS, mean age 48.0 divided into two groups:
n = 50 fallers, mean age 48.8
n = 41 non-fallers mean age 46.7 years
Gait measures The MS fallers presented a higher variability score in the step length and single support compared to participants in the non-fallers. Gait variability scores were significantly correlated with clinical walking tests. 5
Khan et al. 2018,
Qatar [60]
To determine the prevalence and severity of neuropathic pain, sudomotor dysfunction and abnormal vibration perception in patients with MS Design not reported;
n = 73 PwMS, mean age 36.68
Disability, neuropathic pain, sudomotor function, vibration perception threshold Patients with multiple sclerosis have evidence of sudomotor dysfunction and elevated vibration perception. 4
Kjolhede et al. 2015, Denmark [61] To investigate the relationship between rate of force development (RFD) and maximal muscle strength of knee extensors and flexors and measures of functional capacity in PwMS Clinical trial;
n = 35 PwMS, mean age 43.3
Muscle strength, walking, stair climb, functional capacity Rate of force development and maximal muscle strength correlated with functional capacity. Correlations were strongest for knee extensors and flexors of the weaker leg. 4
Larson et al. 2013,
Greece [62]
To quantify bilateral differences in lower-limb performance and metabolism during exercise. Design not reported:
n = 8 PwMS, mean age 51.6
Muscle strength, walking Individuals with MS had significant between-leg differences in leg strength, peak oxygen uptake, and peak workload. 4
McLoughlin et al.
2014,
Australia [63]
To investigate the effect of walking-induced fatigue on lower limb strength and postural sway in people with moderately disabling MS. Controlled study;
n = 34 PwMS, mean age 49.1
Fatigue, postural sway, lower limb strength Significant time by condition effects for all assessment measures indicated the six-minute walk induced fatigue with associated increases in postural sway and reductions in lower limb strength in people with MS. 4
Medina-Perez et al.
2016,
Spain [64]
To examine the effects of 12 wk. of muscle power training on peak muscle power and maximal voluntary isometric contraction (MVIC) of knee extensors in patients with MS Intervention study;
n = 40 PwMS: divided into two groups
n = 20 women with MS, mean age 42.8
n = 20 men with MS, mean age 44.0
Muscle strength No significant changes in the control group from baseline to post-intervention evaluation. In contrast, the exercise group significantly increased MVIC and muscle power after the training. 5
Motl et al. 2012,
USA [65]
To examine changes in walking function associated with combined exercise training consisting of aerobic, resistance, and balance activities in persons with MS who had recent onset of gait impairment Design not reported;
n = 13 PwMS, mean age 51.5
Walking, function These results suggest that a moderately intense, comprehensive, combined exercise training program represents a rehabilitation strategy that is associated with improved walking mobility. 4
Neamtu et al. 2012,
Romania [66]
To present morpho-functional limb aspects during gait at MS patients. Design not reported;
n = 13 PwMS, mean age 36
Biomechanical examination of the foot Load and impulse had high values at MS patients; these patients displayed a significant right-left asymmetry during all the gait phases due to the lower propulsion force of the foot in stride. 3
Nogueira et al. 2013,
Brazil [67]
To analyze the gait characteristics of MS patients in the absence of clinical disability Case-control study;
n = 12 PwMS, mean age 30.6
Disability, gait, perceived balance confidence, physical activity and fatigue MS patients showed impairment of perceived fatigue, perceived of walking impact and perceived balance confidence, despite having no disability. 4
Pau et al. 2015,
Italy [68]
To characterize the gait patterns of individuals with Multiple Sclerosis (MS) affected by spasticity using quantitative gait analysis. Cross-sectional study;
n = 38 PwMS, divided into two groups:
n = 19 PwMS affected by lower limb spasticity, mean age 54.6
n = 19 PwMS not affected, mean age 47.1
Walking, range of motion, muscular activation Spasticity originates a peculiar gait pattern characterized by reduced speed, cadence, stride length, swing phase and increased double support time, but they also reveal specific alterations in kinematics and muscular activation. 4
Pau et al. 2017,
Italy [69]
To quantitatively assess the effect of 6 months of supervised adapted physical activity (APA i.e. physical activity designed for people with special needs) on spatio-temporal and kinematic parameters of gait in persons with Multiple Sclerosis (pwMS) Randomized controlled trial;
n = 22 PwMS, were randomly assigned:
n = 11 intervention group, mean age 47.4
n = 11 control group, mean age 44.5
Gait analysis, range of motion The training originated significant improvements in stride length, gait speed and cadence in the intervention group, while GPS and GVS scores remained practically unchanged. A trend of improvement was also observed as regard the dynamic ROM of hip, knee, and ankle joints. 4
Peruzzi et al. 2017,
Italy [70]
To examine the effect of a virtual reality-based training on gait of people with multiple sclerosis. Single blind randomized controlled trial n = 25 PwMS divided into two groups:
n = 11 control group, mean age 42.0
n = 14 experimental group, mean age 43.6
Gait analysis, clinical motor tests, walking endurance and speed, mobility, balance, obstacle negotiation, disability Subjects in both the groups significantly improved the walking endurance and speed, cadence and stride length, lower limb joint ranges of motion and powers, during single and dual task gait. Subjects in the experimental group also improved balance, as indicated by the results of the clinical motor tests. 5
Picelli et al. 2017,
Italy [71]
To compare the clinical and ultrasonographic features of spastic equinus in patients with chronic stroke and multiple sclerosis Observational study;
n = 38 PwMS, mean age 53.2
n = 38 chronic stroke patients, mean age 61.4
Muscle spasticity Affected calf muscles tone was significantly greater in patients with chronic stroke as well as spastic gastrocnemius muscle echo intensity. Affected ankle range of motion was significantly greater in patients with multiple sclerosis as well as spastic gastrocnemius muscle thickness. 4
Pike et al. 2012,
France, Germany, Italy, Spain, the UK [44]
To evaluate the prevalence, severity and burden of walking and mobility problems (WMPs) in 5 European countries Cross-sectional study, patient record-based study;
n = 2171 PwMS, mean age 40.6
Mobility, walking WMPs were regarded as the most bothersome symptom by almost half of patients. There was a clear, independent and strong directional relationship between severity of WMPs (subjective and objective) and healthcare resource utilisation. Patients with longer walking times (indicating greater walking impairment) were significantly more likely to require additional caregiver support, visit a variety of healthcare professionals including their primary care physicians and require more long-term non-disease modifying drug. 5
Ramdharry et al.
2006,
UK [72]
To evaluate the effects of dynamic foot orthoses (DFO) on walking and balance performance in people with multiple sclerosis (MS). Design not reported;
n = 16 PwMS, age not reported
Walking speed, balance Dynamic foot orthoses may increase sway and change centre of pressure position by altering foot alignment and/or plantar afferent stimulation. 5
Remelius et al. 2012,
USA [73]
To investigate (1) whether previously observed changes in gait parameters in individuals with multiple sclerosis (MS) are the result of slower preferred walking speeds or reflect adaptations independent of gait speed; and (2) the changes in spatiotemporal features of the unstable swing phase of gait in people with MS. Cross-sectional study;
n = 19 PwMS, mean age 51.3
Gait analysis Longer dual support time is part of a gait strategy in MS that is apparent even when controlling for the confounding effect of slower preferred speed. 4
Renfrew et al.
2019
UK [74]
To compare the clinical- and cost-effectiveness of ankle-foot orthoses (AFOs) and functional electrical stimulation (FES) over 12 months in people with Multiple Sclerosis with foot drop. Multicentre, powered, non-blinded, randomized trial;
n = 85 PwMS divided into
n = 43 AFO group,
n = 42 FES device group
Walking speed Both devices demonstrated improvements in walking speed at 12 months, although there were no significant differences in their effects. 4
Rivera-Domingues et al.
1978,
USA [75]
To study the prevalence of the foot deformities pes cavus and claw toes found in spastic spinal cord injury and multiple sclerosis patients and to discuss the pathogenesis of these foot deformities with the help of electromyography. Design not reported;
n = 20 PwMS, mean age 38
n = 80 spinal cord injury patients, mean age 43
Spasticity, foot assessment Pes cavus and claw toes were found in two of 20 multiple sclerosis patients. All patients were spastic and had equinus deformity. 4
Rodgers et al. 1999,
USA [76]
To examine the influence of an aerobic exercise program on lower extremity kinematics and kinetics during gait in patients with MS who demonstrate a range of disability Design not reported;
n = 18 PwMS, mean age 43.2
Range of motion, gait analysis Hip passive range of motion increased. Mean walking velocity, cadence, and posterior shear push-off force decreased. During walking, maximum ankle dorsiflexion decreased and ankle plantarflexion increased. Results suggest this 6-mo training program had minimal effect on gait abnormalities. 4
Romberg et al. 2004,
Finland [77]
To improve walking and other aspects of physical function with a progressive 6-month exercise program in patients with multiple sclerosis (MS). Randomized controlled two-center intervention study;
n = 47 PwMS, exercise group, mean age 43.8
n = 48 PwMS, control group, mean age 43.9
Walking speed, lower extremity strength, upper extremity endurance and dexterity, peak oxygen uptake, static balance. Change between groups was significant in the 7.62 m and 500 m walk tests. In the 7.62 m walk test, 22% of the exercising patients showed clinically meaningful improvements. 4
Rusu et al. 2014,
Romania [78]
Focus on biomechanical foot analyses of MS patients. Clinical research;
n = 48 PwMS, mean age 46.04
Biomechanical foot assessment An instability left to right to be more evident in the swing phase and it influences the under the foot impulse for the next step and postural control. 4
Sandroff et al. 2013,
USA [79]
To examine the associations among aerobic capacity, balance, and lower-limb strength asymmetries, walking performance, and gait kinematics in 31 persons with MS and 31 matched controls. Design not reported;
n = 31 PwMs, mean age not reported (range 18–54 years)
Peak aerobic capacity, muscular strength, balance, walking performance Aerobic capacity, balance, and knee-extensor asymmetry were associated with walking performance and gait in persons with MS. Aerobic capacity and lower-limb strength asymmetries, but not balance, explained significant variance in walking performance and gait kinematics in the MS sample. 4
Solaro et al. 2006,
Italy [80]
To evaluate the frequency of oedema of the lower limbs in multiple sclerosis(MS) patients utilizing a multidisciplinary approach Design not reported;
n = 205 PwMs, mean age 50.53
Assessment for presence of oedema or cutaneous complications. Ninety-three patients (45%) showed oedema at the examination. EDSS, disease duration and disease course, but not gender, were statistically different between oedema and non-oedema patients 5
Sosnoff et al. 2011,
USA [81]
To examine the hypothesis that persons with MS who had spasticity of the lower limbs would have more impairment of mobility and balance performance than persons with MS who did not have spasticity Design not reported;
n = 34 PwMS, mean age 57.5
Spasticity in muscles, walking speed, mobility, walking endurance, self-reported impact of MS on walking ability, balance Fifteen participants had spasticity of the gastroc-soleus muscles based on modified Ashworth scale scores. The spasticity group had lower median EDSS scores indicating greater disability (P = 0.03). Mobility and balance were significantly more impaired in the group with spasticity compared to the group without spasticity. 4
Thoumie et al. 2002,
France [82]
To evaluate the correlation between gait speed and strength in multiple sclerosis (MS) with particular regard to patients presenting with proprioceptive loss Design not reported;
n = 20 PwMS, mean age 42 years
Gait, muscle strength Gait speed was reduced and strongly related to hamstring peak torque but not with quadriceps peak torque. In the patients with proprioceptive loss there was both a strong correlation between gait speed and hamstring torque and a significant correlation with quadriceps torque. 4
White et al. 2004,
USA [83]
To evaluate the effect of an eight-week progressive resistance training programme on lower extremity strength, ambulatory function, fatigue and self-reported disability in multiple sclerosis (MS) patient Experimental study;
n = 8 PwMS, mean age 46
Isometric strength, walking, fatigue, disability Knee extension, plantarflexion and stepping performance increased significantly. Self-reported fatigue decreased and disability tended to decrease following the training programme. 4
Yildiz et al. 2012, Switzerland [84] To identify the relevance and impact of walking speed (WS) over a short distance on activities of daily living (ADLs) in patients with multiple sclerosis (MS). Survey study;
n = 112 PwMS, mean age not reported
Impact of MS on walking Half of participants reported a high impact of MS on their general walking ability and their ability to increase WS over a short distance. Up to 53% of participants reported avoiding ADLs because of concerns about WS. 5