gait characteristics of multiple sclerosis patients in the absence of clinical disability

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Disability & Rehabilitation, 2013; 35(17): 1472–1478© 2013 Informa UK, Ltd.ISSN 0963-8288 print/ISSN 1464-5165 onlineDOI: 10.3109/09638288.2012.738760

Purpose: Motor deficits in lower extremities and gait abnormalities are a major feature of the multiple sclerosis (MS) patients. Patients with minimal clinical disability have subtle gait changes. The aim of this study was to analyze the gait characteristics of MS patients in the absence of clinical disability. Method: A case–control study was carried out with 12 MS patients and 12 matched healthy controls. The subjects underwent a clinical neurological evaluation to determine their disability level (EDSS ≤ 1.5). Then, the subjects were referred for completion self-report questionnaires (gait, perceived balance confidence, physical activity and fatigue), gait clinical trials, and 3D kinematic analysis. Results: MS patients showed more impairment of perceived fatigue, perceived of walking impact and perceived balance confidence, despite having no disability. Gait characteristics showed no differences when they were determined by clinical observation. The 3D kinematic analysis of gait showed slight but significant changes in ankle movement. Conclusion: MS patients with no clinical disability have discrete changes in gait that can be evidenced by perceived impact on walking and kinematic evaluation, mainly of ankle movement. Moreover, there is a decrease in perceived balance confidence and an increase in perceived fatigue, which are correlated despite having different origins.

Keywords: Gait, kinematics, mobility, multiple sclerosis

Introduction

Motor deficits in lower extremities and gait abnormalities are a major feature of the multiple sclerosis (MS) patients [1]. Mobility problems are present in 75% of MS patients [2]. Lower limb function was given the highest priority, followed by visual functioning and cognition, especially in longer

lasting MS [3]. Gait was the main physical outcome that nega-tively affected MS patients’ quality of life [4]. Slower walking speed at baseline was the most significant predictor of disease progression in the primary progressive form of MS over 10 years [5].

Gait analysis of MS patients can be performed through self-report questionnaires [2], clinical tests [2,4–8], or kinematic analysis [1,9–11]. The gold standard of assessment is three-dimensional motion analysis integrating kinematic, kinetic, and electrophysiological measurements; however, this technology is often not readily accessible for routine analyses, being time-consuming and expensive in terms of both infrastructure and resources [12]. In MS, there is some evidence to suggest that even for patients with minimal neurological signs on clinical examination (Expanded Disability Status Scale – EDSS < 3.0), there are subtle gait and postural control changes [1,10], and those findings may therefore be indicative of compromised walking stability [10]. During the gait cycle, MS patients change the joint motion patterns in the sagittal plane at the hip, knee, and ankle [1]. Even patients without impairment of habitual walking show changes in gait kinematics [1,10].

RESEARCH PAPER

Gait characteristics of multiple sclerosis patients in the absence of clinical disability

Leandro Alberto Calazans Nogueira1,2, Luciano Teixeira3, Pollyane Sabino1, Helcio Alvarenga Filho1, Regina Maria Papais Alvarenga1 & Luiz Claudio Thuler1,4

1Neurology Postgraduate Program, Federal University of Rio de Janeiro State, Rio de Janeiro, Brazil, 2Federal Institute of Education, Science and Technology of Rio de Janeiro, Rio de Janeiro, Brazil, 3Physical Therapy of Gaffrée e Guinle University Hospital, Rio de Janeiro, Brazil, and 4National Cancer Institute (INCA), Rio de Janeiro, Brazil

Correspondence: Luiz Claudio Thuler, Departamento de Neurologia, Hospital Universitário Gaffrée e Guinle, Rua Mariz e Barros, 775 – Rio de Janeiro, CEP.: 20270-004, Brazil. Tel: 55-21-2264-2123. Fax: 55-21-2264-2123. E-mail: [email protected]

Disability & Rehabilitation

2013

35

17

1472

1478

© 2013 Informa UK, Ltd.

10.3109/09638288.2012.738760

0963-8288

1464-5165

Gait in MS patients with no disability

08October2012

• Multiple sclerosis patients showed changes in gait pat-tern even with no clinical disability.

• The reduction of plantar flexion movement at toe off may be the first compensatory strategy on early phases of disease.

• Fatigue, higher walking impact, and less balance con-fidence are early symptoms of Multiple Sclerosis.

Implications for Rehabilitation

(Accepted October 2012)

L. A. C. Nogueira et al.

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Gait in MS patients with no disability 1473


Benedetti et al. [1] analyzed patients with mild disability (EDSS ≤ 2) and showed a decrease of speed in free walking compared to controls because of reductions in both stride length and cadence. A prolonged double support phase and an arrhythmic gait were also observed. Other researches also reported the same results, and so far, to the best of our knowledge, there is no study of gait analysis in MS patients in the absence of clinical disability (EDSS ≤ 1.5). The aim of this study was to analyze the gait characteristics of MS patients in the absence of clinical disability.

Methods

ParticipantsA case–control study was carried out with two groups of subjects (MS patients and controls). Data were collected at the Physical Therapy Clinic of Gaffrée and Guinle University Hospital (GGUH), Rio de Janeiro, Brazil. Twelve subjects diagnosed with MS (average age: 30.6 years; average height: 168 cm; average mass: 67.17 kg; gender: 9 females and 3 males; average IPAQ: 3221.75) and 12 healthy control sub-jects (average age: 33.2 years; average height: 169 cm; aver-age mass: 68.17 kg; gender: 9 females and 3 males; average IPAQ: 3874.62) participated in this study. The patients were recruited from the outpatient clinic of GGUH, and a control group of healthy subjects were recruited from the staff and student community of the Physical Therapy department. The inclusion criteria consisted of a diagnosis of MS according to the criteria established by McDonald et al. [13] and presented no disability on the Expanded Disability Status Scale (EDSS ≤1.5). The exclusion criteria include patients with other forms of idiopathic demyelinating disease, patients currently undergoing an MS attack, and patients with another associ-ated neurological disease. The control subjects were healthy adults with a negative clinical diagnosis of MS and no reports of neurologic impairments. Subjects from the MS group were matched with subjects from the control group based primarily on gender and age, followed by an agreement between subject pairs in height, weight, and physical activity level. The study was approved by the Human Research Ethics Committees of GGUH, and all subjects provided informed consent prior to their participation.

InstrumentsDisabilityA disability is defined as a condition or function judged to be significantly impaired relative to the usual standard of an individual or group. The term is used to refer to individual functioning, including physical impairment, sensory impair-ment, cognitive impairment, intellectual impairment, mental illness, and various types of chronic disease. In the present study, a standardized bedside neurologic examination was performed by a neurologist. The scores obtained in this examination allowed neurologic impairment and disability to be established using the Expanded Disability Status Scale (EDSS). Clinicians determine a patient’s EDSS level by first assigning a separate grade for eight functional systems, including pyramidal, cerebellar, bowel and bladder, cerebral,

brain stem, sensory, visual, and other functions. A composite of grades is then used to determine an individual’s EDSS score, ranging from 0 (normal neurologic exam) to 10.0 (death due to MS) [14]. The EDSS is the most widely used scale for MS disability and is a commonly used rating system for evaluating the degree of neurologic impairment in MS based on neuro-logic findings.

Gait questionnaireThe MSWS-12 is a 12-item self-report measurement of the impact of MS on walking. The items are rated on a 5-point scale of 1 (Not at all) to 5 (Extremely) and represent limita-tions in walking during the past 2 weeks. The MSWS-12 is scored by summing the item scores, subtracting 12 from the sum, dividing the difference by 60, and then multiplying the result by 100. The scores range between 0 and 80, and higher scores indicate worse walking mobility or more walking dif-ficulty. The MSWS-12 has good evidence for internal consis-tency, test–retest reliability, and validity of scores as a measure of walking mobility in MS [2].

Gait clinical trialParticipants were instructed to walk barefoot at their self-selected, comfortable speed along a 14-m walkway. A ‘‘dynamic start’’ was used where the subject may accelerate 2 m before entering the timed 10-m distance and decelerate 2 m afterwards. As long as subjects are able to ambulate the required 14 m, they are able to participate in the test. Timing was started when the lead foot crossed the starting and was stopped when the lead foot crossed the finish line. Speed was only calculated for the 10-m distance between the starting and the finish line to avoid measuring the acceleration and deceleration phases of gait. The second walking trial was recorded to minimize the learning effect. The walking time and the number of steps were registered. Then the gait speed, cadence, step, and stride length were estimated. The 10-m timed walk test (10-m TWT) is valid and reliable for patients with neurologic impairment [15].

3D kinematic analysisVideo analyses were performed simultaneously in the same environment. A tridimensional analysis was performed with four video camera recordings (Kodak Zi10 sampled at 60 frames per second). Data were collected across the central 4 m of the walkway to exclude the acceleration and decelera-tion phases of each trial. To evaluate the hip, knee, and ankle kinematics during gait, 15 adhesive markers were attached to the subjects to define the thigh, shank, and foot segments, according to the Helen Hayes protocol previously described for gait analysis [16]. The same examiner placed the mark-ers. The Hu-m-an software (HMA Technology) was used for video analysis. For three-dimensional analysis, the software accepts two-dimensional source digitized data and uses a direct linear transform to produce the 3D coordinate file. A gait cycle was digitized and synchronized for each subject. The swing phase, stance phase, double support duration (% gait cycle), and hip, knee, and ankle kinematic data were measured.

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1474 L. A. C. Nogueira et al.


Physical activityPhysical activity was measured with the short form of the International Physical Activity Questionnaire (IPAQ), which was designed for population surveillance of physical activity among adults. The IPAQ short form has 6 items that measure the frequency and duration of vigorous-intensity activities, moderate-intensity activities, and walking during a 7-day period. The respective frequency values for vigorous, mod-erate, and walking activities were multiplied by 8, 4, and 3.3 metabolic equivalents and then summed to form a continuous measure of physical activity. Weikert et al. [17] found a strong correlation between IPAQ scores and accelerometer move-ment counts in persons with MS. The IPAQ was validated for use in the Portuguese language [18].

FatigueFatigue was assessed by the Modified Fatigue Impact Scale (MFIS), which is a 21-item self-report multidimensional scale developed to assess the perceived impact of fatigue on a vari-ety of daily activities over the previous 4 weeks. The items of the MFIS can be aggregated into three subscales (Physical, Cognitive, and Psychosocial), as well as into a total MFIS score. The MFIS total score is the sum of the three subscales and range from 0 to 84. All items are scaled so that higher scores indicate a greater impact of fatigue on a patient’s activities. Values below 38 indicate absence of fatigue. The reliability and validity of the MFIS have been established in patients with MS, and the MFIS was validated for use in the Portuguese language [19].

Perceived balance confidencePerceived Balance Confidence was assessed by the Activities-Specific Balance Confidence (ABC) Scale. This 16-item scale requires respondents to self-rate their balance confidence in performing activities of daily living from 0% to 100%. Averaging the ratings derives total scores, and higher scores reflect higher levels of balance confidence. The ABC Scale has been used with various populations and has psychometric evidence supporting its use with MS patients. It was validated for use in the Portuguese language [20].

ProceduresAfter providing informed consent, the subjects underwent a clinical neurological evaluation to determine their disability level on the EDSS as an inclusion criterion. Then, the sub-jects were referred for completion of self-report question-naires, gait clinical trials, and 3D kinematic analysis. Gait was assessed by three tests: MSWS-12, 10-m TWT, and 3D kinematic analysis. The use of video analysis software is an efficient approach to improve the reliability of visual video assessments [12]. In addition to gait analysis, the physical activity level, perceived impact of fatigue, and perceived bal-ance confidence were evaluated as a possible factors associ-ated with gait performance. Assessments were made in the morning since changes in fatigue and gait had been described from morning to afternoon [21].

Data analysisNormal probability plots were inspected for each variable. The data distribution of each variable was verified through

the Shapiro–Wilk test. Comparison between the groups was performed using the non-paired Student’s t test or the Mann Whitney U test. The chi-square test was used to analyze cat-egorical variables. Pearson and Spearman rank correlations were performed for MS group variables when appropriate. A two-way analysis of covariance (ANCOVA) was used to examine the influence of demographic and clinical character-istics that were statistically different between the groups. The significance level was established at 5% (p < 0.05). A power analysis was performed for the main kinematic result. All data were analyzed using the Statistical Package for the Social Sciences (SPSS, Inc., Chicago, IL) version 17.0 software.

Results

Twenty-four subjects participated in the study: 12 MS patients with no disability and 12 matched healthy controls. Independent samples t-tests indicated that the subject groups were not significantly different in age, height, mass, gender, and physical activity level measures. The only difference found was in perceived fatigue, which was higher in the patients. The values are described in Table I.

Four patients presented normal neurological exam, and six patients presented minimal signs in one Functional System (FS). Only two patients presented minimal signs in more than one FS. Pyramidal FS was the most affected and showed 58% of patients with no disability having abnormal signs. The val-ues are described in Table II.

Despite having no disability, the patient had a more severe perceived walking impairment than controls. The patients also showed a decrease in perceived balance confidence. Gait speed, step length, double support duration and swing phase duration showed no statistically significant differences between the groups. Cadence showed a tendency to be higher in patients, but this result was not statistically significant (Table III). Female patients showed an average gait speed of 1.28 m/s (SD ± 0.26) and had an average age of 29.67 years, while male patients showed an average gait speed of 1.21 m/s (SD ± 0.16) and had an average age of 32.67 years. Non-pyramidal patients showed an average gait speed of 1.38 m/s (SD ± 0.20), while pyramidal patients showed an average gait speed of 1.18 m/s (SD ± 0.25).

Kinematic analysis was performed only in the right lower limb because there were no differences in symmetry (right swing time/left swing time) between the patients and controls. The results revealed no difference in most of the movements analyzed: hip and knee angle at heel contact, hip and knee angle at toe off, maximal hip and knee flexion, and maximal hip and knee extension. However, the ankle angle at heel contact (MS group = −6.08, SD ± 3.40, 95% CI [4.16–8.01] × Control group = −12.83, SD ± 9.29, 95% CI [7.58–18.09]; p = 0.03, power = 0.71), toe off (MS group = −25.75, SD ± 6.03, 95% CI [22.34–29.16] × Control group = −35.50, SD ± 10.28, 95% CI [29.68–41.32]; p = 0.01, power = 0.91), and maximal plantiflexion (MS group = −29.75, SD ± 7.42, 95% CI [25.55–33.95] × Control group = −38.33, SD ± 12.23, 95% CI [31.41–45.25]; p = 0.04, power = 0.68) showed a significant difference. Figure 1 shows the ankle kinematic

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profile for the MS and control group. The knee angle at heel contact was more flexed in the MS group (MS group = 10.58, SD ± 8.64 × Control group = 1.58, SD ± 13.74; p = 0.07), but this difference was not statistically significant.

Correlation analysis was performed only in MS patients. Strong correlations were observed between fatigue and per-ceived impact on walking (rho = −0.87, p < 0.01), between fatigue and perceived balance confidence (rho = −0.73, p < 0.01), and between perceived impact on walking and per-ceived balance confidence (rho = −0.71, p < 0.01).

Since the only difference was found in perceived fatigue, ANCOVA was used to examine the influence of fatigue on gait and perceived balance confidence. ANCOVA analysis was performed with the group as a categorical variable, fatigue as a covariate, and perceived impact on walking, perceived bal-ance confidence, and ankle kinematics as dependent variables.

The only difference between patients and controls that remained statistically significant (p = 0.02) was in ankle move-ment; there was no difference in perceived impact on walking (p = 0.46) and perceived balance confidence (p = 0.18), indi-cating interaction between fatigue and these characteristics.

Discussion

The groups were matched by gender, age, BMI, and physical activity level to avoid the influence of confounding factors.

The present study seems to be the first to analyze the gait characteristics of MS patients, taking into account that the participants were matched on physical activity level. Other authors have reported on the influence of physical activity level on gait performance in MS patients [22,23]. Even with substantial effort to match the groups, gait abnormalities were observed in patients compared to controls, both in perceived impact on walking and in kinematic analysis. Evidence of gait abnormalities in MS patients with mild [7] and minimal [1,10,24] disability has been described. Recent data showed balance control modifications in patients diagnosed with clinically isolated syndrome suggestive of MS [25] and MS patients who walk at normal speeds showed dynamic balance impairment [26].

The perceived fatigue was increased in patients; the analysis of covariance revealed no interaction between the fatigue and ankle motion, but an influence of fatigue on perceived impact on walking and perceived balance confidence. Thus, the 3D kinematic assessment was the only measure that detected dif-ferences in the gait of patients in the absence of clinical disabil-ity. Several authors have shown increased fatigue in MS patients and have suggested the involvement of central nervous system [27] and the possibility of fatigue being a primary condition of MS, although its origin is not clearly understood. Huisinga et al. [28] found a correlation between fatigue, measured by the Fatigue Severity Scale, and deficits in ankle power generation at late stance despite the higher perception of fatigue severity in those mild disability participants (average EDSS = 2.6) com-pared to the present study (MFIS 42.3 × 18.58, respectively). Sacco et al. [29] found a correlation between temporal-spatial parameters of gait (speed, cadence, and stride length) and fatigue and disability, but this result remains contradictory. As in the present study, Morris et al. [21] and Crenshaw et al. [30] found no correlation between fatigue and walking speed, step length, and double support time even after induction of additional fatigue [31]. These findings support the idea that the mechanisms controlling locomotion are separate from those regulating perceived fatigue [21]. The findings of Sacco et al. [29] may be associated with deconditioning status once the sample is admitted for inpatient rehabilitation.

The 10-m TWT was not enough to detect gait abnormali-ties, perhaps due to the sample characteristics (no disabilities), which contributed to a ceiling effect of the test. The present

Table I. Demographic and clinical data of the MS and control group.MS (n = 12) (mean ± SD)

Control (n = 12) (mean ± SD) p value

Age (years) 30.56 (±5.01) 33.17 (±7.28) 0.33Gender (female/male) 9:3 9: 3 1.00Weight (kg) 67.17 (±13.07) 68.17 (±17.15) 0.87Height (m) 1.68 (±0.10) 1.69 (±0.09)BMI 23.16 (±3.16) 23.00 (±3.67) 0.90Number of falls (total) 2 1 0.65MFIS 18.58 (±15.04) 6.83 (±9.12) 0.03*IPAQ 3,221.75

(±2517.73)3,874.62 (±5026.76) 0.91

IPAQ Classification Low – 2; Moderate – 1;

High – 9

Low – 2; Moderate – 1; High – 9

1.00

BMI, body mass index; IPAQ, International Physical Activity Questionnaire; MFIS, Modified Fatigue Impact Scale.*Significance level < 0.05.

Table II. Kurtzke’s functional system evaluation (n = 12).Subject EDSS Visual Brainstem Pyramidal Cerebellar Sensory Bowel and bladder Cerebral (mental) Other1 1 0 0 1 0 0 0 0 02 0 0 0 0 0 0 0 0 03 1 0 0 1 0 0 0 0 04 1 0 0 1 0 0 0 0 05 1.5 1 1 1 0 0 0 0 06 1 1 0 0 0 0 0 0 07 0 0 0 0 0 0 0 0 08 1.5 0 0 1 1 1 0 0 09 0 0 0 0 0 0 0 0 010 1 0 0 1 0 0 0 0 011 1 0 0 1 0 0 0 0 012 0 0 0 0 0 0 0 0 0

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gait speed data, measured by the 10-m TWT, were classified as normal gait speed when compared to the gender and age normative data described by Bohannon et al. [32]. Spain et al. [26] also described that MS patients who walk at normal speeds and control subjects groups were indistinguishable when tested for gait speed, cadence, swing, and double sup-port time using the timed walk test. Several authors reported gait clinical abnormalities, such as in speed [1,6,7,21,29,30] and cadence [1,7,21,29]. Most studies assessed patients with mild (EDSS ≤ 3) [1,7,10] or moderate disability (EDSS ≤6.5) [6,8,29]. MS patients with minimal disability, determined by EDSS evaluation, walked slower, with fewer, shorter and wider steps and spent a greater percentage of a gait cycle with two feet on the ground [24].

Givon et al. [7] found that gait speed and double support time correlated with neurological disability and the pyrami-dal functional score (PFS). In the present study, this corre-lation was not observed since the patients had no disability (EDSS ≤ 1.5). Martin et al. [10] found a slight reduction in gait speed (gait speed PFS = 1.10 m/s × non-PFS = 1.1 m/s), in patients with PFS impairment when compared to patients with non-PFS impairment (gait speed PFS = 1.18 m/s × non-PFS = 1.38 m/s). In the presence of disability, the questionnaire

(MSWS-12) and 10-m TWT have proven effective in identi-fying abnormal gait in MS patients [33]and have been used in management therapy with good results [9,29], yet in the absence of clinical disability in MS patients these measures could not detect some deficits.

The kinematic analysis of gait showed slight but significant changes in ankle movement. Some authors have observed greater variability of hip, knee, and ankle motion in MS patients compared with controls [11,30], even with mild disability [1]. Martin et al. [10] evaluated patients with and without PFS impairment and reported differences in ankle movement, but patients with EDSS ≤2.5 were included. Our results showed that even in subjects with no disability (EDSS ≤ 1.5) and matched on physical activity level, the plantar flex-ion movement at toe off is still decreased. The reduced range of motion and power generation of the ankle at toe off is an important finding in patients with traumatic brain injury, healthy elderly, and stroke populations [34] and has also been observed in MS [28]. The reduced plantar flexion range of motion at toe off maybe the first modification of gait pattern in MS patients, and a progressive worsening of ankle move-ment over time may lead to hip flexion increase, gait speed reduction, shorter steps, or shorter terminal stance phase.

In MS, changes in ankle movement may be caused by somatosensory impairment and/or motor impairments, such as spasticity and muscle weakness. MS patients have a reduc-tion in light touch and pressure plantar sensation [11], and their postural variability of the center of pressure is greater in the anteroposterior direction compared to controls [6]. It has been suggested that the anteroposterior direction of balance is controlled by ankle strategy. Eils et al. [35] demonstrated that reduced plantar sensation in a group of healthy adults leads to significant changes in gait kinematics at the ankle, knee, and hip joint and indicates a more cautious ground contact and push-off with modified EMG and motion patterns. Given that the pyramidal subscore of the EDSS was the most common impairment in the present study, it was hypothesized that gastrocnemius-soleus muscle spasticity and muscle weakness could contribute to a reduction of ankle movement. Kelleher et al. [36] conducted an ambulatory rehabilitation review and considered spasticity as a primary factor affecting ambula-tion. Sosnoff et al. [37] evaluated patients with mild to mod-erate disability (EDSS: 3.5–7.0) and found that spasticity in the gastrocnemius-soleus muscles appears to have a negative effect on mobility, balance performance, and self-reported balance ability. Lower values of plantar flexion at toe off can be caused by muscle weakness due to spasticity or somatosensory impairment even in MS patients with no disability. Thoumie et al. [38] found a strong correlation between gait velocity and strength of the hamstrings and quadriceps regardless of the clinical form in patients with MS.

The participants of the present study showed higher bal-ance confidence and less walking impact than those described in other researches. This result was expected since the study investigated patients with no disability. The initial group dif-ferences in patient’s perceived balance confidence and per-ceived impact on walking disappeared when an ANCOVA was performing. The ANCOVA was done to increase statistical

Table III. Comparison of perceived impact on walking, perceived balance confidence and temporal-spatial characteristics between MS patients and controls.

MS (n = 12) (mean ± SD)

Control (n = 12) (mean ± SD) p value

MSWS-12 7.5 (±11.54) 0 (0) 0.02*Balance confidence 94.73 (±5.03) 98.93 (±2.02) 0.02*Gait speed (m/s) 1.27 (±0.24) 1.19 (±0.10) 1.00Cadence (steps/min) 117.21 (±12.93) 110.79 (±5.38) 0.08Step length (cm) 0.65 (±0.09) 0.65 (±0.04) 0.92Double support duration (% gait cycle)

24.08 (±3.85) 24.81 (±4.12) 0.66

Swing phase duration (% gait cycle)

37.25 (±2.70) 36.50 (±2.43) 0.48

MSWS-12, Multiple Sclerosis Walking Scale-12.*Significance level < 0.05.

Figure 1. Ankle kinematic profile for the MS and control groups. The solid and dotted lines, respectively, represent the MS group mean ± 1SD; the grey band represents the control group (mean ± 1SD). The two ver-tical lines indicate toe off (TO) for the control (c) group (mean 65.1% stride). Heel strike (HS) occurs at 0% and 100% of the stride.

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power and revealed an interaction with patient’s perceived fatigue in those differences. The group differences found may reflect the disease impairment since the three characteristics were measured by self-reported questionnaires. The correla-tion analysis in this study showed close relationship between gait, patient’s perceived balance confidence, and fatigue according to the high values found for these variables. The changes in gait reported in people with MS are consistent with their reported changes in balance control [39]. The differences may reflect a more cautious walking strategy due to dynamic balance impairment. Spain et al. [26] found that the angular trunk range of motion was significantly larger in MS patients who walk at normal speeds than controls in both roll (medio-lateral flexion) and yaw (axial trunk rotation) axes.

A potential weakness of this study may be the small num-ber of participants, although the power analysis revealed power to be greater than 0.9 to plantar flexion movement at toe off and other researches on gait analyses in MS popula-tions have found that the ankle joint is the most affected. The second possible limitation is that we did not find any gait research in MS patients with no disability (EDSS ≤ 1.5) with which to compare data. The patients had Functional System abnormalities that could contribute to some differences, although the only study that performed such analysis found similar results between pyramidal and non pyramidal MS patients [10]. Finally, the neurologic clinical examination and EDSS were not sufficient to detect some motor impairment that is more appropriately investigated with laboratory gait analysis. Despite these limitations, the intriguing results pro-vide impetus for future research. Studies with larger sample sizes that include participants with greater disability and dif-ferent functional system impairments from those in the pres-ent study should be undertaken to confirm the present results.

Conclusions

This study showed that MS patients with no clinical disability have discrete changes in gait that can be evidenced by per-ceived impact on walking and kinematic evaluation, mainly of ankle movement. Moreover, there is a decrease in perceived balance confidence and an increase in perceived fatigue, which are correlated despite having different origins.

Acknowledgements

Special thanks to Dr. Rafael Bahamonde for gait technical help and to Dr. Bruno Silva for statistical assistance.

Declaration of Interest: The authors report no conflicts of interest.

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gait characteristics of multiple sclerosis patients in the absence of clinical disability

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