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Walking and Thinking in Persons With Multiple Sclerosis Who Vary in Disability

      Abstract

      Sosnoff JJ, Boes MK, Sandroff BM, Socie MJ, Pula JH, Motl RW. Walking and thinking in persons with multiple sclerosis who vary in disability.

      Objective

      To examine the effect of a cognitive task on spatiotemporal parameters of gait in persons with multiple sclerosis (MS) with varying disability.

      Design

      Cohort.

      Setting

      Testing occurred at a local hospital.

      Participants

      Community-living persons (N=78) with MS participated in this investigation. They were divided into 3 groups based on Expanded Disability Status Scale (EDSS) scores: mild (2.0–3.5 EDSS; n=21); moderate (4.0–5.5 EDSS; n=25); and severe (6.0–6.5 EDSS; n=32).

      Interventions

      Not applicable.

      Main Outcome Measures

      Participants walked at a self-selected pace on an electronic pathway, which recorded spatiotemporal parameters of gait, in 4 separate trials and completed a cognitive task in the last 2 trials. The effect of the cognitive task was quantified as the change in spatiotemporal parameters of gait.

      Results

      There was an overall decline in gait with the additive cognitive task. The magnitude of the adverse changes ranged from 1.8% for step length (P=.02) to 12% for gait velocity (P<.001). Moreover, adverse changes in gait function were greatest in the severe and moderate disability group (P<.05).

      Conclusions

      Persons with MS have impaired walking while doing a cognitive task, and the adverse effect of a cognitive task on walking function is greatest in persons with severe and moderate disability. Difficulty walking while thinking has implications for everyday life and may be related to the risk of falls. Further work is needed to determine whether the adverse effect of an additive cognitive task can be minimized with rehabilitative interventions.

      Key Words

      List of Abbreviations:

      CIS (clinically isolated syndrome), CNS (central nervous system), DTC (dual task cost), EDSS (Expanded Disability Status Scale), FAP (functional ambulatory profile), MS (multiple sclerosis), WLG (word list generation)
      MULTIPLE SCLEROSIS (MS) is a chronic, potentially disabling neurologic disease common among adults worldwide and in the United States. The relapsing form of disease involves episodes of focal inflammation in the central nervous system (CNS)
      • Hemmer B.
      • Nessler S.
      • Zhou D.
      • Kieseier B.
      • Hartung H.P.
      Immunopathogenesis and immunotherapy of multiple sclerosis.
      that result in demyelination and possible transection of axons. This progressive axonal damage produces conduction delay along neuronal pathways throughout the CNS
      • Bjartmar C.
      • Trapp B.D.
      Axonal and neuronal degeneration in multiple sclerosis: mechanisms and functional consequences.
      and eventually results in accumulation of cognitive and physical disability.
      Cognitive dysfunction is common in MS. Approximately 65% of persons with MS have cognitive dysfunction.
      • Maurelli M.
      • Marchioni E.
      • Cerretano R.
      Neuropsychological assessment in MS: clinical, neurophysiological and neuroradiological relationships.
      • Chiaravalloti N.D.
      • DeLuca J.
      Cognitive impairment in multiple sclerosis.
      All cognitive domains are affected in persons with MS, and the pattern of impairment seems to be heterogeneous.
      • Calabrese P.
      Neuropsychology of multiple sclerosis—an overview.
      The domains of information processing ability, working memory, and attentional capacity are especially compromised.
      • Calabrese P.
      Neuropsychology of multiple sclerosis—an overview.
      Cognitive impairment often occurs early in disease, even in persons with minimal disability, and may antagonize physical disability such as walking function.
      Walking is impaired in MS, with upwards of 85% of patients reporting gait as a primary limitation.
      • Scheinberg L.
      • Holland N.
      • Larocca N.
      • Laitin P.
      • Bennett A.
      • Hall H.
      Multiple sclerosis; earning a living.
      Walking impairment has been documented with tests of walking endurance and speed,
      • Kragt J.J.
      • van der Linden F.A.
      • Nielsen J.M.
      • Uitdehaag B.M.
      • Polman C.H.
      Clinical impact of 20% worsening on timed 25-foot walk and 9-hole peg test in multiple sclerosis.
      • Goldman M.D.
      • Marrie R.A.
      • Cohen J.A.
      Evaluation of the six-minute walk in multiple sclerosis subjects and healthy controls.
      • Hobart J.
      • Freeman J.
      • Thompson A.
      Kurtzke scales revisited: the application of psychometric methods to clinical intuition.
      • Noseworthy J.H.
      Clinical scoring methods for multiple sclerosis.
      as well as with spatiotemporal markers of gait.
      • Thoumie P.
      • Lamotte D.
      • Cantalloube S.
      • Faucher M.
      • Amarenco G.
      Motor determinants of gait in 100 ambulatory patients with multiple sclerosis.
      • Givon U.
      • Zeilig G.
      • Achiron A.
      Gait analysis in multiple sclerosis: characterization of temporal-spatial parameters using GAITRite functional ambulation system.
      For example, with the use of an electronic pathway that provides an overall functional ambulatory profile (FAP) score as well as common spatiotemporal markers, the overall FAP score and other spatiotemporal markers were found to be compromised in persons with MS versus control subjects. Further, the FAP score was negatively associated with the Expanded Disability Status Scale (EDSS) score in persons with MS.
      • Givon U.
      • Zeilig G.
      • Achiron A.
      Gait analysis in multiple sclerosis: characterization of temporal-spatial parameters using GAITRite functional ambulation system.
      Traditionally, walking impairment in persons with MS has been associated with dysfunction within the neuromuscular system. For example, leg muscle strength
      • Thoumie P.
      • Lamotte D.
      • Cantalloube S.
      • Faucher M.
      • Amarenco G.
      Motor determinants of gait in 100 ambulatory patients with multiple sclerosis.
      and spasticity
      • Kelleher K.J.
      • Spence W.
      • Solomonidis S.
      • Apatsidis D.
      The characterisation of gait patterns of people with multiple sclerosis.
      have been associated with walking impairment in MS. There is emerging evidence that cognition might be associated with impaired walking in MS.
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      • Kalron A.
      • Dvir Z.
      • Achiron A.
      Walking while talking—difficulties incurred during the initial stages of multiple sclerosis disease process.
      One study
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      reported that performing a cognitive task while walking (ie, performing a dual task) resulted in a significant reduction in walking performance (eg, decreased velocity, increased double-support phase) in persons with MS versus control subjects, and this dual task cost (DTC) has been observed early in the disease.
      • Kalron A.
      • Dvir Z.
      • Achiron A.
      Walking while talking—difficulties incurred during the initial stages of multiple sclerosis disease process.
      Although some researchers have suggested that DTC is not associated with disability,
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      the sample for this proposition had minimal disability (eg, EDSS score <3.0). Consequently, there is no evidence either supporting or refuting the possibility that the DTC is affected by the degree of disability status in persons with MS.
      This investigation examined the effect of a cognitive task on gait performance in persons with MS who had mild, moderate, and severe disability. It was expected that persons with greater disability, as indexed by the EDSS,
      • Kurtzke J.F.
      Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS).
      would have greater impairments in walking function, and that the walking impairment would become more pronounced while performing a cognitive task (ie, greater DTC) than it would for persons with MS who had mild or moderate disability.

      Methods

      Participants

      The sample consisted of 78 persons who were recruited through 3 locally residing neurologists. To be included in the investigation, participants had to have a neurologist-confirmed diagnosis of MS; the ability to walk independently or with a cane, crutch, or walker; understand written and spoken English; and be relapse free for 30 days. Participants were divided into 3 groups based on EDSS scores. The mild disability group had EDSS scores between 2.0 and 3.5 (n=21), the moderate disability group had EDSS scores between 4 and 5.5 (n=25), and the severe disability group had EDSS scores between 6.0 and 6.5 (n=32). MS type, age, sex, education, MS duration, disease-modifying treatments, EDSS score, and use of an assistive device across the 3 groups are reported in table 1. There was no difference between groups in disease duration (F2,75=1.2; P=.28), sex composition (χ2=0.3; P=.87), MS type (χ2=2.8; P=.25), and disease-modifying therapies (χ2=1.8; P=.40). As expected, the groups differed on EDSS (χ2=722.2; P<.001) and assistive device use (χ2=28.0; P<.001). The moderate and severe disability groups were less educated than the mild disability group (χ2=6.6; P<.05). Per definition of EDSS, all members of the severe disability group used an assistive device, whereas members of the other groups did not use assistive devices (see table 1). There was a difference between groups in age (F2,75=16.8; P<0.00; η2=.31). Post hoc analysis revealed that the severe disability group was older than the mild disability group (d=–1.69) (see table 1). The demographic characteristics of the sample reflect the general MS population.
      • Mayr W.T.
      • Pittock S.J.
      • McClelland R.L.
      • Jorgensen N.W.
      • Noseworthy J.H.
      • Rodriguez M.
      Incidence and prevalence of multiple sclerosis in Olmsted County, Minnesota, 1985-2000.
      Table 1Participant Demographics
      VariableMildModerateSevereF Ratio/χ2P
      Age (y)43.3±10.753.3±8.558.0±8.216.8.00
      Yr-Dx10.2±7.010.7±9.213.8±11.91.4.28
      Sex (F/M)17/420/424/80.8.87
      Education (median)College degreeSome collegeSome college6.2.04
      EDSS2.5 (.75)4.5 (.50)6.0 (.25)722.2.00
      MS type19 RR/2 PP20 RR/2 PP/2 SP21 RR/6 PP/3 SP2.8.25
      Disease-modifying treatments1822242.1.40
      Assistive device (n)003228.0.00
      NOTE. Values are mean ± SD, median (interquartile range), or as otherwise indicated.
      Abbreviations: F, female; M, male; PP, primary progressive; RR, relapse remitting; SP, secondary progressive; Yr-Dx, years since diagnosis.

      Procedures

      Upon arrival to the neurology clinic, the experimental procedures were discussed with the participants, who then read and provided written informed consent. Participants further provided demographic information, and we measured their height and weight using a scale stadiometer. All participants then underwent a neurologic examination by a neurologist, who then generated an EDSS score. In brief, the EDSS score assesses function in 8 functional systems including the pyramidal, cerebellar, brainstem, sensory, bowel and bladder, visual, mental, and other. It is commonly used as an outcome measure in clinical trials. EDSS scores range from 0 to 10, with 0 representing no neurologic impairment, 2.0 representing minimal disability in one functional system, 4.0 reflecting the onset of walking impairment, 6.0 corresponding to the requirement of unilateral assistance (eg, cane or crutch), 8.0 indicating that the individual is unable to walk and is restricted to bed, and 10.0 is death caused by MS.
      • Kurtzke J.F.
      Rating neurologic impairment in multiple sclerosis: an Expanded Disability Status Scale (EDSS).
      • Kurtzke J.F.
      Natural history and clinical outcome measures for multiple sclerosis studies Why at the present time does EDSS scale remain a preferred outcome measure to evaluate disease evolution?.
      Participants next completed 4 walking trials on a 26-foot GAITRite electronic walkwaya at a comfortable pace with or without an assistive device (eg, cane, walker). Participants began each walking trial 5ft in front of the mat and walked 5ft past the end of the mat to promote a constant walking speed during each trial. During the first 2 trials, participants did not perform a cognitive task, whereas in the second 2 trials, participants completed a modified word list generation (WLG) task while walking. Participants were given the opportunity to rest between trials. The modified WLG is a commonly used assessment in neuropsychological tests for cognitive impairment in MS
      • Boringa J.B.
      • Lazeron R.H.
      • Reuling I.E.
      • et al.
      The brief repeatable battery of neuropsychological tests: normative values allow application in multiple sclerosis clinical practice.
      and has been used to examine DTCs in previous research on MS.
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      The WLG task involved participants stating as many words in a certain category (eg, animals, words that began with the letter “D”) in a certain amount of time. The first dual task trial used a semantic word generation task (ie, participants were instructed to list as many fruits and vegetables as possible when walking on the mat), while the second dual task trial used a phonetic word generation task (ie, participants were asked to name as many words beginning with the letter “D” as possible when walking on the mat). The use of both semantic and phonetic tasks minimized any potential for a learning effect. The number of words uttered was recorded and normalized by walking time, to account for different walking speeds across disability groups.
      The initial and final steps of each trial were excluded from data analyses based on manufacturer suggestions. On average, 21 steps were analyzed for each trial. Participants were provided with rest breaks between trials to minimize any effects of fatigue.
      For a given trial, the GAITRite software a calculated the overall FAP score and normalized velocity (via leg length) along with stride length, step time, base of support, percentage of gait cycle spent in double-support phase (double support), and percentage of gait cycle spent in swing phase (swing) for each individual leg. For brevity, we averaged each parameter across legs. The average of each of these variables for each walking condition was used in the analysis for improved reliability of the measures.
      DTC was calculated, based on the procedures of Hamilton et al,
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      as the percent change from single (walking) to dual (walking and cognitive task) task performance for each variable of interest.
      DTC=([SD]/S)*100


      where S is equal to single task performance and D is equal to dual task performance. A positive DTC indicates a decrease in performance with the cognitive task for FAP score, velocity, cadence, step length, and swing phase. A negative DTC indicates a decrease in performance with the cognitive task for step time and percentage of gait cycle spent in double support.

      Statistical Analysis

      Descriptive analyses were performed in SPSS version 17.0.b The main analysis involved a 1-way analysis of variance, with disability group as the between-subjects factor. Significance was noted when the P value was less than .05. The magnitude of the group main effect was expressed using partial η2, and Cohen's guidelines of .01, .06, and .14 were used for judging the η2 values as small, moderate, and large, respectively.
      • Cohen J.
      Statistical power analysis for the behavioral sciences.
      Main effects were decomposed using post hoc analyses with a correction of α. We further expressed between-group differences in mean scores using Cohen's d, and values of .2, .5, and .8 were used for judging the effect sizes as small, moderate, and large, respectively.
      • Cohen J.
      Statistical power analysis for the behavioral sciences.
      Single sample t tests were used to determine whether there was an overall DTC for all variables (ie, significantly different than the value of 0). Values are mean ± SD unless otherwise noted (eg, median for EDSS).

      Results

      Performance on the WLG normalized to ambulation time (number of utterances per ambulation time) was influenced by group (F2,75= 5.5; P =.00; η2=.13). Post hoc analysis revealed that the mild disability group listed more words while walking than the severe disability group (1.1 vs .73 words/s; d=1.05).
      Spatiotemporal parameters of gait as a function of disability level in the normal walking condition (ie, no cognitive task) are reported in table 2. As expected, the severe disability group had significantly worse walking characterized by a lower FAP score (79.1 vs [mild] 94.7 and [moderate] 91.4), slower velocity (78.4cm/s vs [mild] 133.9cm/s and [moderate] 105.6cm/s), fewer steps (94.5 steps/min vs [mild] 116.2 steps/min and [moderate] 106.0 steps/min), shorter (48.6cm vs [mild] 68.9cm and [moderate] 58.5cm) and wider (14.4cm vs [mild] 9.9cm and [moderate] 12.5cm) steps, a greater percentage of each gait cycle in double support (34.8% vs [mild] 27.7% and [moderate] 31.3%) compared with the other groups, and a lower percentage of each gait cycle in swing phase (31.7% vs [mild] 36.2% and [moderate] 34.5%). Effect sizes (η2) for the group main effect were generally large, ranging from .15 to .54. Post hoc analysis revealed that the group main effect resulted from differences between each disability group with gait impairment scaling with disability group, with moderate to large effect sizes (Cohen's d) ranging from .44 to 2.3.
      Table 2Spatiotemporal Parameters of Gait as a Function of Disability Level in Normal Walking Conditions
      VariableMildModerateSevereF RatioPη2
      FAP94.7±6.991.4±10.579.1±13.315.1.00.29
      Velocity (cm/s)133.9±19.8105.6±24.378.4±19.543.2.00.54
      Cadence (steps/min)116.2±10.1106.0±12.494.5±12.321.7.00.37
      Step length (cm)68.9±8.258.5±10.948.6±11.723.4.00.39
      Step time (s)0.52±0.030.56±0.050.67±0.1112.5.00.40
      Double support (% gait cycle)27.7±3.831.3±4.834.8±4.624.7.00.40
      Swing phase (% gait cycle)36.2±2.534.5±2.831.7±3.714.0.00.28
      Base of support (cm)9.9±5.212.6±4.114.4±3.96.6.00.15
      NOTE. Values are mean ± SD or as otherwise indicated.
      To determine the overall effect of the dual task on walking performance, the DTC for each variable was compared with zero. As noted in table 3, there was a significant alteration in gait with the cognitive task. Specifically, there was a statistically significant positive DTC for FAP score (t=4.9), velocity (t=11.6), cadence (t=10.7), and step length (t=2.5), indicating a decrease in these metrics with the cognitive task. The changes ranged from 1.8% for step length to 11.8% for velocity of single task performance. There was a statistically significant negative DTC for bilateral step time (t=−5.5) and percentage of gait cycle spent in double support (t=−4.1), indicating an increase in these measures with the cognitive task. The changes ranged from −3.0% for double support percentage to −4.5% for step time of single task performance. There was no significant DTC for percent of gait cycle spent in the swing phase (t=1.5) and base of support (t=0.3).
      Table 3Overall DTC of Spatiotemporal Parameters of Gait
      VariableDTC (%)tP
      FAP5.8±7.74.9.00
      Velocity11.8±8.911.6.00
      Cadence7.6±6.210.7.00
      Step length1.8±6.42.5.01
      Step time−4.5±7.6−5.5.00
      Double support−3.0±6.3−4.1.00
      Swing phase0.9±5.01.3.10
      Base of support1.5±18.60.3.76
      NOTE. Values are mean ± SD or as otherwise indicated.
      The effect of disability level on DTC is seen in table 4. Statistical analysis revealed a group effect for FAP score, velocity, and cadence, with overall effect sizes (η2) ranging from .10 to .16. Post hoc analysis revealed that the group main effect resulted from the severe disability group having greater dual cost in FAP score, velocity, and cadence compared with the mild disability group, with moderate to large effect sizes (Cohen's d) ranging from 0.7 to 1.2. In addition, the moderate group had a greater DTC in FAP, velocity, and cadence compared with the mild group (d value range, 0.7–1.1). Overall, these observations suggest that disability level impacts the magnitude of DTCs. The effect of disability level on DTC remained when controlling for age.
      Table 4DTC as a Function of Disability Group
      VariableMildModerateSevereF RatioPη2
      FAP DTC (%)0.3±8.37.5±8.15.7±7.84.9.01.12
      Velocity DTC (%)7.2±6.913.4±9.813.6±8.64.1.02.10
      Cadence DTC (%)3.5±4.39.4±7.88.9±4.77.0.00.16
      Step length DTC (%)1.7±5.22.4±6.91.6±6.00.2.85.01
      Step time DTC (%)−1.8±4.7−7.7±7.8−6.7±8.03.9.02.10
      Double support DTC (%)−1.7±7.5−3.5±6.2−4.0±6.31.3.29.03
      Swing phase DTC (%)0.2±2.82.0±3.50.2±6.41.1.31.03
      Base of support DTC (%)4.2±32.31.5±17.6−2.1±10.40.6.55.02
      WLG (no. of words/s)1.1±0.30.9±0.20.7±0.35.5.00.14
      NOTE. Values are mean ± SD or as otherwise indicated.

      Discussion

      This investigation examined the effect of a cognitive task on gait performance in persons with MS across varying levels of disability. Congruent with previous reports,
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      • Kalron A.
      • Dvir Z.
      • Achiron A.
      Walking while talking—difficulties incurred during the initial stages of multiple sclerosis disease process.
      there was a decrease in walking function while simultaneously performing a cognitive task in persons with MS. The novel observation of this investigation was that the reduction in walking function was greatest in persons with severe disability compared with persons with minimal disability. This observation is in direct contrast with the proposition that DTCs are unrelated to disability progression in persons with MS.
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.

      Walking and MS

      As expected, there were differences in walking function between disability groups.
      • Givon U.
      • Zeilig G.
      • Achiron A.
      Gait analysis in multiple sclerosis: characterization of temporal-spatial parameters using GAITRite functional ambulation system.
      • Kelleher K.J.
      • Spence W.
      • Solomonidis S.
      • Apatsidis D.
      The characterisation of gait patterns of people with multiple sclerosis.
      • Sosnoff J.J.
      • Weikert M.
      • Dlugonski D.
      • Smith D.C.
      • Motl R.W.
      Quantifying gait impairment in multiple sclerosis using GAITRite technology.
      Compared with the mild and moderate disability groups, the severe disability group walked slower, with shorter steps, and spent a greater percentage of the gait cycle in double support. Deficits in walking function in persons with MS are multifaceted, with muscle weakness,
      • Thoumie P.
      • Lamotte D.
      • Cantalloube S.
      • Faucher M.
      • Amarenco G.
      Motor determinants of gait in 100 ambulatory patients with multiple sclerosis.
      fatigue,
      • Sacco R.
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      • Kesselring J.
      • Beer S.
      Assessment of gait parameters and fatigue in MS patients during inpatient rehabilitation: a pilot trial.
      and spasticity
      • Kelleher K.J.
      • Spence W.
      • Solomonidis S.
      • Apatsidis D.
      The characterisation of gait patterns of people with multiple sclerosis.

      Sosnoff JJ, Gappmeir E, Frame A, Motl RW. Spasticity, mobility and balance in persons with MS. J Neurol Phys Ther. In press.

      all reported as contributing factors. In essence, the observed group differences in spatiotemporal parameters indicate that the grouping of participants based on walking impairment was successful. The increase in walking dysfunction seen between disability groups may stem from an increase in these or other factors, such as cognitive deficits, with increases in disability level.

      DTC and Walking

      Overall, participants demonstrated a decrease in walking performance while simultaneously performing a cognitive task, in line with previous research. Kalron et al
      • Kalron A.
      • Dvir Z.
      • Achiron A.
      Walking while talking—difficulties incurred during the initial stages of multiple sclerosis disease process.
      examined DTC during walking using a modified word generation task in 52 persons with clinically isolated syndrome (CIS) who were minimally impaired compared with healthy age- and sex-matched control subjects. There was a greater DTC in persons with CIS compared with healthy control subjects. Importantly, the reported DTCs of an approximately 7% decrease in walking velocity and a 3% decrease in cadence are similar to those reported for the mild disability group in the current study.
      Using a memory task, Hamilton
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      reported a 9% decrease in gait velocity in minimally impaired persons with MS (mean EDSS, 2.74), which was significantly greater than that in healthy control subjects. Hamilton
      • Hamilton F.
      • Rochester L.
      • Paul L.
      • Rafferty D.
      • O'Leary C.P.
      • Evans J.J.
      Walking and talking: an investigation of cogntiive-motor dual tasking in multiple sclerosis.
      reported no association between disease severity and DTC, although the authors did downplay this conclusion because of a minimally disabled sample, as cane use was an exclusion criterion. In the current investigation, which examined persons with MS who had a broad range of disability (EDSS range, 2.0–6.5; median, 5.0), DTC was found to be associated with disability level. Indeed, the severe and moderate disability group had DTC that was 2 to 3 times greater than the mild disability group. These group differences were only apparent for gait velocity, FAP score, and cadence.
      There are 2 main theoretic models used to explain a decrease in walking function with an additive cognitive task: the capacity model and bottleneck model.
      • Woollacott M.
      • Shumway-Cook A.
      Attention and the control of posture and gait: a review of an emerging area of research.
      The capacity model maintains that there are finite cognitive resources available, and decrements in performance ensue once demands outpace the cognitive capacity available. The bottleneck model maintains that there is a reduction in performance when similar cognitive/neural pathways are used simultaneously. Although the current investigation was not designed to test either of these predictive models, the capacity model conceptually fits with the well-established impairments in cognitive function seen in persons with MS.
      • Chiaravalloti N.D.
      • DeLuca J.
      Cognitive impairment in multiple sclerosis.
      • Calabrese P.
      Neuropsychology of multiple sclerosis—an overview.
      Although it is logical to assume that the neural pathways required for word generation do not overlap with that of gait, it has been suggested that verbal fluency tasks, such as the task used here, share complex neural pathways connecting different brain regions that are interlinked with those controlling gait.
      • Al-Yahya E.
      • Dawes H.
      • Smith L.
      • Dennis A.
      • Howells K.
      • Cockburn J.
      Cognitive motor interference while walking: a systematic review and meta-analysis.
      More research is needed to test these contrasting hypotheses.
      There are several reasons why the severe disability group had a large DTC. For instance, there is evidence that cognitive function declines with disease progression, as indexed by disability in persons with MS.
      • Maurelli M.
      • Marchioni E.
      • Cerretano R.
      Neuropsychological assessment in MS: clinical, neurophysiological and neuroradiological relationships.
      • Calabrese P.
      Neuropsychology of multiple sclerosis—an overview.
      • Lynch S.G.
      • Parmenter B.A.
      • Denney D.R.
      The association between cognitive impairment and physical disability in multiple sclerosis.
      • Patti F.
      • Amato M.P.
      • Trojano M.
      • et al.
      Cognitive impairment and its relation with disease measures in mildly disabled patients with relapsing-remitting multiple sclerosis: baseline results from the Cognitive Impairment in Multiple Sclerosis (COGIMUS) study.
      As such, it is possible the severe disability group had decreased cognitive capacity, and the additive cognitive task resulted in greater dysfunction. Although not specifically tested here, the severe disability group's poor performance on the WLG task is indicative of decreased cognitive capacity. It is also possible that there were no differences in cognitive capacity between groups, but rather the severe and moderate disability groups, because of their increased walking impairment, required greater cognitive resources to walk. A related, but slightly different argument is that the use of an assistive device (eg, cane, walker) places an additional cognitive demand on walking. In the gerontology literature, it has been reported that older adults require greater cognitive resources for walking while using an assistive device than walking without an assistive device.
      • Wellmon R.
      • Pezzillo K.
      • Eichhorn G.
      • Lockhart W.
      • Morris J.
      Changes in dual-task voice reaction time among elders who use assistive devices.
      Given that all participants in the severe disability group used an assistive device and none in the mild disability group used one, it is possible that the greater dual cost for the severe disability group stems from the increased cognitive demands of using an assistive device. However, the moderate group, who did not use assistive devices, had an elevated DTC compared with the mild disability group, thus minimizing this possibility. Further work is needed to gain a better understanding of the interaction between disability and dual task demands.
      In addition, it is possible that the effect of disability on DTC could be mediated by another factor. It is well known that older adults have an increased DTC compared with young adults.
      • Woollacott M.
      • Shumway-Cook A.
      Attention and the control of posture and gait: a review of an emerging area of research.
      • Al-Yahya E.
      • Dawes H.
      • Smith L.
      • Dennis A.
      • Howells K.
      • Cockburn J.
      Cognitive motor interference while walking: a systematic review and meta-analysis.
      • Bock O.
      Dual-task costs while walking increase in old age for some, but not for other tasks: an experimental study of healthy young and elderly persons.
      Given that the severe disability group was significantly older than the mild disability group, it is possible that aging and not disability per se is driving the relation. To test this possibility, the analyses were repeated while controlling for age. Overall, the effect of disability group on DTC was still apparent when age was taken into account. Further, although the moderate disability group had a significantly greater DTC than the mild disability group, there were no significant differences in age between these groups. We propose that disability, separate from age, is driving the enhanced DTC seen in the severe and moderate disability groups.

      Significance of DTC

      Regardless of the factors contributing to dual task impairments in persons with MS, it presents a significant issue. An approximately 10% decrease in gait speed might negatively impact activities of daily living (eg, shopping or crossing a busy intersection). Moreover, the DTC of walking (ie, reduction in gait velocity) has been shown to be predictive of recurrent falls in older adults
      • Beauchet O.
      • Annweiler C.
      • Allali G.
      • Berrut G.
      • Herrmann F.R.
      • Dubost V.
      Dual task-related changes in gait performance in older adults: a new way of predicting recurrent falls?.
      and associated with fall risk in persons with Parkinson's disease.
      • Hausdorff J.M.
      • Balash J.
      • Giladi N.
      Effects of cognitive challenge on gait variability in patients with Parkinson's disease.
      Although falls are a significant problem for persons with MS,
      • Finlayson M.L.
      • Peterson E.W.
      • Cho C.C.
      Risk factors for falling among people aged 45 to 90 years with multiple sclerosis.
      the association between falls and DTC in MS is unknown. There is evidence that indirectly suggests that DTC is related to falls in persons with MS. Nilsagard et al
      • Nilsagard Y.
      • Lundholm C.
      • Denison E.
      • Gunnarsson L.G.
      Predicting accidental falls in people with multiple sclerosis—a longitudinal study.
      has shown that performance of a timed up and go task while engaging in a cognitive task is partially predictive of falls in persons with MS. The researchers did not specifically determine DTC per se, so it remains to be seen whether DTCs are associated with falls in persons with MS.
      There is growing evidence that DTCs can be improved with training in older adults and persons with Parkinson's disease.
      • Canning C.G.
      • Ada L.
      • Woodhouse E.
      Multiple-task walking training in people with mild to moderate Parkinson's disease: a pilot study.
      • Silsupadol P.
      • Shumway-Cook A.
      • Lugade V.
      • van Donkelaar P.
      • Chou L.S.
      • Mayr U.
      • Woollacott M.H.
      Effects of single-task versus dual-task training on balance performance in older adults: a double-blind, randomized controlled trial.
      For instance, Brauer and Morris
      • Brauer S.G.
      • Morris M.E.
      Can people with Parkinson's disease improve dual tasking when walking?.
      recently demonstrated that acute dual task training can improve some aspects of walking function in persons with Parkinson's disease. It is well known that walking function can be improved with various rehabilitation techniques in persons with MS.
      • Kraft G.H.
      Rehabilitation still the only way to improve function in multiple sclerosis.
      • Romberg A.
      • Virtanen A.
      • Ruutiainen J.
      • et al.
      Effects of a 6-month exercise program on patients with multiple sclerosis: a randomized study.
      There is some limited evidence that cognitive function can be improved with targeted interventions.
      • O'Brien A.R.
      • Chiaravalloti N.
      • Goverover Y.
      • Deluca J.
      Evidenced-based cognitive rehabilitation for persons with multiple sclerosis: a review of the literature.
      Indirectly, the benefits of rehabilitation on walking and cognition suggest that DTC in persons with MS can be minimized with targeted interventions. However, this possibility requires additional scientific scrutiny.

      Study Limitations

      An important limitation in the current investigation is that performance in the cognitive task was not examined while participants were not ambulating. As such, it is possible that the differences in DTC between disability groups stem from the groups focusing on different tasks (eg, walking or cognitive task). However, it has been suggested that walking is the de facto prime task because of the importance of mobility and avoiding falls.
      • Woollacott M.
      • Shumway-Cook A.
      Attention and the control of posture and gait: a review of an emerging area of research.
      Another limitation is that the non–dual task trials were always completed before the completion of the dual task trials. Consequently, it is possible that participants were more fatigued during the dual task trials than the non–dual task trials. Moreover, given the association between fatigue and disability in persons with MS,
      • Mills R.J.
      • Young C.A.
      The relationship between fatigue and other clinical features of multiple sclerosis.
      it is logical to speculate that more disabled participants had greater fatigue and therefore more impaired walking during the later trials. Although the influence of fatigue is a possibility, its influence was minimized experimentally by allowing participants to rest after each trial. In addition, the walking bouts were relatively short (∼25ft) and self-paced. Further work is needed to examine the influence of fatigue on DTC in persons with MS. Additional limitations include the uneven sample size between groups and the lack of a control group.

      Conclusions

      The current observations are noteworthy by providing novel empirical evidence that disability level impacts the DTC in persons with MS. Research examining the factors underlying DTC in persons with MS is warranted. In addition, further work is necessary to determine whether targeted interventions can minimize DTC in persons with MS.
      • a
        CIR Systems, Inc. 60 Garlor Dr, Havertown, PA 19803.
      • b
        SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

      Acknowledgments

      We thank the staff of the Illinois Neurologic Institute at OSF Hospital; Madeline Weikert, Swathi Balantrapu, and Yoojin Suh for help with data collection; and Emily Berman for assistance with database management.

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