Walking while talking—Difficulties incurred during the initial stages of multiple sclerosis disease process

doi:10.1016/j.gaitpost.2010.06.002

Gait & Posture

Volume 32, Issue 3, July 2010, Pages 332-335

https://doi.org/10.1016/j.gaitpost.2010.06.002 Get rights and content

Abstract

Patients with multiple sclerosis (MS) frequently experience poor gait and/or cognitive impairment, even in the early stages of the disease. As gait is often executed simultaneously with different cognitive tasks, it is essential to test gait during a cognitive load. Therefore, the main objective of this study was to assess gait and gait variations while simultaneously performing a cognitive task in patients with a clinically isolated syndrome (CIS) suggestive of MS. Fifty-two CIS patients, aged 33.8 ± 0.2 years with an Expanded Disability Status Scale (EDSS) score of 1.7 ± 0.2 were included in the study. The control group consisted of 28 age- and gender-matched healthy subjects. Major spatio-temporal parameters were collected via an electronic walkway (GAITRite electronic walkway system). Participants were instructed to walk under three different conditions: normal, fast, and at a normal pace while performing the modified word list generation (WLG) test. Compared to healthy subjects, the CIS patients’ gait was slower and asymmetrical with a wider base of support. The combined walking and cognitive task was expressed in prolonged double support (% gait cycle) and reduced velocity in patients only. As these findings are associated with the very early phase of MS, it appears that the ongoing pathological disease process is already taking place with regard to gait abilities. Since in early MS patients, gait-cognitive dual tasking may lead to an increased risk of falling, this important function should be addressed by physical rehabilitation clinicians.

Introduction

Multiple sclerosis (MS) is an autoimmune disease of the central nervous system causing progressive disability in young adults. Most MS patients (85%) complain of disturbances in gait [1] and more than 66% do not retain the ability to walk 20 years after diagnosis [2], [3]. Recently, several studies demonstrated gait deficits early in the disease process, even in relapsing remitting (RR) MS patients with minimal, no gait or balance deficits on clinical examination [4], [5], [6].

Walking has traditionally been considered automatic or reflex controlled, requiring minimal attentional resources, though a recent review suggested that walking control could be attentionally demanding [7]. In order to clarify this issue, various investigation models have tested the interaction of cognitive-walking dual tasks in healthy and patient populations. Dual tasking refers to the ability to perform two actions simultaneously. Studies have researched the effects of executing concurrent cognitive tasks while walking in people with different neurological pathologies, such as Alzheimer's [8] and Parkinson's disease [9]. These studies suggested that speed and accuracy of walking is affected by simultaneously performing a cognitive task. As well as having implications for everyday life, where one is frequently required to do two things at once, dual-tasking difficulties may help explain the high risk of falls [8].

To date there appears to be a few possible explanations for the occurrence of a dual-tasking deficit. One is postulated on basic damage to the motor system eventually leading to a higher demand of conscious attention during the performance of several tasks [10]. Another possibility is that in specific neurological pathologies, working memory capacity is reduced due to overload by previously normal loads of motor and cognitive content [11]. One more possibility is that rather than basic working memory capacity being the problem, a deficit in the attention control system exists, allocating attention between concurrent demands [11].

A recently published case–control study investigated walking and attention interaction in MS patients. Compared to healthy controls, MS patients (n = 18, EDSS = 2.7) demonstrated slower velocity and elevated swing time variability in gait performance under cognitive dual task conditions [12].

The question that should be asked is at which stage of the MS disease process do dual task conditions affect gait performance, specifically which gait parameters are affected and to what extent.

The first neurological presentation suggestive of MS is defined as a clinically isolated syndrome (CIS), with 21% of the patients presenting with optic neuritis, 46% with long tract motor symptoms and signs, 10% with a brainstem syndrome and 23% with multifocal abnormalities [13]. Even at this early disease stage, patients may experience mobility deficits [14]. Previous studies have proven that cognitive dysfunction is also prevalent at the early stages of the disease [15], [16]. Recent research on 67 probable MS patients revealed that following completion of a battery of neuropsychological tests, cognitive impairment was detected in 53.7% of the patients. Verbal abilities and attention span were most frequently affected [17].

Raising awareness, among both professionals and early onset MS patients of potential walking while talking difficulties, is important in order to plan treatment protocols, everyday activities and clinical assessments.

The objective of the present study was to evaluate gait in patients with CIS, up to 3 months from onset, and to determine the effect of a cognitive task on spatio-temporal gait parameters.

Section snippets

Patients and subjects

Fifty-two early onset CIS patients (36 women and 16 men), mean age of 35.2 ± 1.3 years (range 20–45), volunteered to participate in the study. All patients were distinguished by having experienced a first well-defined neurological event consistent with demyelination, confirmed by neurological examination and Fazekas’ criteria of brain MRI [18]. A diagnosis of possible MS was based on Poser's criteria (clinically probable MS C2 or clinically probable MS C3) [19] or according to the revised

Results

The CIS patient group had a mean duration of 54.0 ± 6.2 days since onset of symptoms. The EDSS score was 1.7 ± 0.2 representing minimal neurological disability. Other participant related clinical scores are outlined in Table 1.

Table 2 refers to the gait parameters during normal walking, derived from the system's software program. Significant differences between patients and healthy subjects were associated with step time and length, double support time and width of base of support. Although both

Discussion

In the current study, gait parameter impairment in CIS patients were identified. When compared to healthy subjects, patients walked slower, with larger step asymmetry, with a wider base of support and a prolonged double support period. In accordance with our hypotheses, CIS patients significantly changed gait patterns when performing the walking-cognitive dual task compared to the healthy controls. Furthermore, in contrast to the control group, the patient's gait demonstrated a wider and fixed

Conflict of interest

The authors confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

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Cited by (93)

Cognitive-motor interference in people with mild to moderate multiple sclerosis, in comparison with healthy controls
2022, Multiple Sclerosis and Related Disorders
Reduced motor and cognitive dual-task capacity is found to be more common among people with multiple sclerosis (MS), than among healthy populations. However, studies in larger samples of MS conducted using a more stringent methodology, which includes comparisons to healthy controls, are needed. Thus, the primary aim of this study was to explore the effects on motor and cognitive dual-tasking in people with mild to moderate overall MS-disability, in comparison to healthy controls. A second aim was to explore the differences in dual-task performance on a cognitive task between two motor tasks in people with mild to moderate MS and healthy controls.
This case-control study evaluated dual-task performance of the motor tasks standing with eyes closed (hereafter standing) and walking and a cognitive task assessing selective executive functions (auditory-Stroop test). Fifty-five people with MS (mild MS, n = 28; moderate MS, n = 27), and 30 healthy controls participated. Standing and walking were assessed using wireless inertial measurement unit sensors (APDM). Standing (three 30 s trials) was measured using sway area and root mean square sway, while walking (2 min) was measured using speed, stride length, and step time. Auditory-Stroop was measured using accuracy and response time. During dual-task assessments, each subject was instructed to pay equal attention to both tasks. Statistical significance was considered if p < .05.
In standing no significant within-group differences in the standing measures were found between single-task and dual-task performance. However, dual-task performance differed significantly between all groups (moderate MS > mild MS > healthy controls), except between mild and moderate MS in sway area. In walking, all groups slowed down speed and shortened stride length during dual-task condition compared to single-task condition. Moderate MS performed significantly poorer than mild MS and healthy controls in dual-task walking, but mild MS did not differ from healthy controls. In the cognitive task only mild MS increased significantly in auditory-Stroop response time during walking. In healthy controls, the performance of auditory-Stroop was not affected by dual-tasking. Moderate MS had significantly longer response time in dual-task auditory-Stroop compared to the other groups, but no differences were observed between mild MS and healthy controls. Only mild MS had significantly longer response time during walking than during standing.
This study showed that cognitive-motor interference in people with MS is present also in the early phases of the disease. This was shown during dual-tasking with slower walking and a longer response time in the cognitive task compared to healthy controls. Moderate MS performed poorer in almost every aspect of the motor and cognitive assessments in dual-task condition, compared to mild MS and healthy controls. Furthermore, during standing, people with MS performed poorer in standing measures compared to healthy controls. Additionally, healthy controls showed no cognitive interference during motor tasks.
The results suggest that standardized regular assessment of dual-tasking in MS care might increase the individual's knowledge of dual-task capacity and contribute to understanding of possible related consequences. However, feasible assessment equipment and specific motor-cognitive dual-task training interventions for people with MS need to be developed.
Dual task training effects on gait and balance outcomes in multiple sclerosis: A systematic review
2021, Multiple Sclerosis and Related Disorders
People with Multiple Sclerosis (PwMS) exhibit deteriorated balance and gait performance during dual task (DT) conditions. Impaired dual tasking is related to increased fall risk and lower quality of life in PwMS. While dual task interventions have proven effective in various patient populations, evidence is lacking to support the use of DT interventions to improve clinical measures of balance and gait in PwMS. Therefore, the purpose of this systematic review was to synthesize the effectiveness of DT intervention at improving balance and gait in PwMS.
A systematic search was completed using CINHAL, PubMed and MEDLINE. Methodological quality, level of evidence and recommendations for included studies was assessed by two reviewers. Effect sizes with 95% confidence intervals comparing single and DT outcomes were calculated for all balance and gait variables.
Five randomized control trials (RCTs) were included for review. Of the 23 effect sizes calculated, three had 95% confidence intervals which did not pass zero and were therefore interpreted as strong. Due to inconsistent level one evidence of DT interventions being superior to single task balance and gait interventions a grade B recommendation was given.
There is inconsistent evidence supporting the use of DT interventions to improve clinical balance measures in PwMS. There is supportive evidence for the use of DT interventions to improve both single and DT gait speed. However, there was heterogeneity between interventions and dosage among RCTs. Despite multiple promising findings, DT interventions appear to have minimal impact on clinical balance and gait measures in PwMS.
The patients’ perspective on the perceived difficulties of dual-tasking: development and validation of the Dual-task Impact on Daily-living Activities Questionnaire (DIDA-Q)
2020, Multiple Sclerosis and Related Disorders
Citation Excerpt :
However, there is no consensus on which tasks combination creates higher interference (Leone et al., 2015; Patel et al., 2014). The effects of DT on walking (e.g., reduction of gait velocity, increase of double support duration) (Kalron et al., 2010; Learmonth et al., 2014; Pau et al., 2018) may depend on the type of the concurrent task in MS: for example, many cognitive tasks require a verbal response modality (talking, counting), adding the potential interference of speech articulation on walking. At the same time, different walking and balance requirements under DT condition may produce specific detrimental effects on cognitive performance (Hamilton et al., 2009) or alter the attention allocated to the concomitant tasks (i.e., altered prioritization strategy) in PwMS, depending on the perceived difficulty of the tasks (Allali et al., 2014).
Everyday-life activities often require performing dual tasks (DT), with consequent possible occurrence of motor-cognitive or motor-motor interference. This could reduce quality of life, in particular in people with neurological diseases. However, there is lack of validated tools to assess the patients’ perspective on DT difficulties in this population. Therefore, we developed the Dual-task Impact on Daily-living Activities-Questionnaire (DIDA-Q) and tested its psychometric properties in people with multiple sclerosis (PwMS).
Items were generated based on existing scales, DT paradigms used in previous studies and the opinion of a multi-stakeholder group, including both experts and PwMS. Twenty DT constituted the preliminary version of the DIDA-Q which was administered to 230 PwMS. The psychometric properties of the scale were evaluated including internal consistency, validity and reliability.
Nineteen items survived after exploratory factor analysis, showing a three-factor solution which identifies the components mostly contributing to DT perceived difficulty (i.e., balance and mobility, cognition and upper-limb ability). The DIDA-Q appropriately fits the graded response model, with first evaluations supporting internal consistency (Cronbach's alpha=0.95), validity (70% of the hypotheses for convergent and discriminant constructs confirmed) and reliability (intraclass correlation coefficients=0.95) of this tool.
The DIDA-Q could be used in research and clinical settings to discriminate individuals with low vs. high cognitive-motor or motor-motor interference, and to develop and evaluate the efficacy of personalized DT rehabilitative treatments in PwMS.
A multi-modal virtual reality treadmill intervention for enhancing mobility and cognitive function in people with multiple sclerosis: Protocol for a randomized controlled trial
2020, Contemporary Clinical Trials
Citation Excerpt :
During the dual-task condition, we will use the Modified Word List Generation (WLG) task as the dual-task. This is a previously validated task that tests phonemic verbal fluency and has been found to elicit dual-task interference in MS. [17,39,40] Using standardized procedures, the WLG task will be carried out in the sitting position as a single-task and during walking as a dual-task to determine dual-task costs both with respect to gait and the cognitive task. Dual-task costs will be determined as: [100*(single-task value – dual-task value)/single-task value] both for gait speed and the WLG.
Gait and cognitive impairments are common in individuals with Multiple Sclerosis (MS) and can interfere with everyday function. Those with MS have difficulties executing cognitive tasks and walking simultaneously, a reflection of dual-task interference. Therefore, dual-task training may improve functional ambulation. Additionally, using technology such as virtual reality can provide personalized rehabilitation while mimicking real-world environments. The purpose of this randomized controlled trial is to establish the benefits of a combined cognitive-motor virtual reality training on MS symptoms compared to conventional treadmill training.
This study will be a single-blinded, two arm RCT with a six-week intervention period. 144 people with MS will be randomized into a treadmill training alone group or treadmill training with virtual reality group. Both groups will receive 18 sessions of training while walking on a treadmill, with the virtual reality group receiving feedback from the virtual system. Primary outcome measures include dual-task gait speed and information processing speed, which will be measured prior to training, one-week post-training, and three months following training.
This study will provide insight into the ability of a multi-modal cognitive-motor intervention to reduce dual-task cost and to enhance information processing speed in those with MS. This is one of the first studies that is powered to understand whether targeted dual-task training can improve MS symptoms and increase functional ambulation. We anticipate that those in the virtual reality group will have a significantly greater increase in dual-task gait speed and information processing speed than those achieved via treadmill training alone.
The ability of the instrumented tandem walking tests to discriminate fully ambulatory people with MS from healthy adults
2019, Gait and Posture
People with multiple sclerosis (PwMS) experience walking and balance deficits at the initial phases of the disease, even when classified as only minimally disabled. Complex balance tasks, such as tandem walking, are probably more sensitive in detecting mild balance difficulties compared to the standard traditional tests in this population.
The aim was to investigate different types of 3-meter tandem walking tests in fully ambulatory PwMS.
This observational case-control study included 50 participants; 25 PwMS, 17 women and 8 men, aged 35.2 (S.D = 8.6) and 25 healthy subjects, 18 women and 7 men, aged 34.3 (S.D = 6.1). The 3-meter tandem walk tests were performed during a single session. Each subject completed a sequence of 3 consecutive tests under 3 different task conditions: normal tandem walking, backward tandem walking and cognitive tandem walking. Tandem walking tests were evaluated via three small, lightweight axial wearable accelerometers (APDM, Oregon, USA).
The mean EDSS for the MS group was 1.6 (S.D = 0.6) indicating minimal disability. PwMS walked slower and at a slower pace, with a prolonged double support and decreased swing phase compared to healthy subjects in normal and backward conditions. In contrast, during the cognitive task, non-significant differences were found in gait measures between the PwMS and the healthy controls. Significant differences were found between task conditions for all participants. All reduced their walking speed and walked at a slower pace in both the cognitive and backward conditions compared to the normal tandem walk condition. However, non-significant scores were found for the condition X group factor.
The study provides new insights into the 3-meter tandem walk test. Findings should improve evaluation and training of dynamic balance in fully ambulatory PwMS.
Spinal cord involvement in multiple sclerosis and neuromyelitis optica spectrum disorders
2019, The Lancet Neurology
Spinal cord involvement is an important cause of disability in patients with multiple sclerosis or neuromyelitis optica spectrum disorders (NMOSDs). Multiple sclerosis and NMOSDs can be distinguished from other disorders that cause myelopathy by results from laboratory and radiological investigations. However, limitations in the sensitivity and specificity of spinal cord imaging and poor correlation with disability megasures have impeded the understanding of the relationship between spinal cord involvement and clinical manifestations. Nevertheless, studies of the pathological features of multiple sclerosis and NMOSDs have shown that quantitatively different mechanisms lead to differences in clinical course and pattern of accrual of permanent disability in the two disorders. Better understanding of these mechanisms is necessary to develop more informative clinical measures, electrophysiological methods, fluid biomarkers, and imaging techniques to detect and monitor spinal cord involvement in the diagnosis and management of patients with multiple sclerosis or NMOSDs, and as outcome measures in clinical trials.

View all citing articles on Scopus

^☆: This work was performed in partial fulfillment of the requirements for a Ph.D. degree of Alon Kalron, Sackler Faculty of Medicine, Tel Aviv University, Israel.

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Walking while talking—Difficulties incurred during the initial stages of multiple sclerosis disease process☆

Abstract

Introduction

Section snippets

Patients and subjects

Results

Discussion

Conflict of interest

Gait Posture

Gait Posture

Rev Neurol (Paris)

Gait Posture

Arch Clin Neuropsychol

J Neurol Sci

Gait Posture

Multiple sclerosis; earning a living

NY State J Med

The natural history of multiple sclerosis: a geographically based study. I. Clinical course and disability

Brain

Multiple sclerosis. A rehabilitation approach to management

Gait abnormalities in minimally impaired multiple sclerosis patients

Mult Scler

Gait and balance impairment in early multiple sclerosis in the absence of clinical disability

Mult Scler

Dual tasking, gait rhythmicity, and Parkinson's disease: which aspects of gait are attention demanding?

Eur J Neurosci

Is there evidence for a specific executive capacity for dual task co-ordination? Evidence from Alzheimer's disease

Neuropsychology

Walking and talking: an investigation of cognitive-motor dual tasking in multiple sclerosis

Mult Scler