The Presence, Type, and Burden of Walking, Gait, and Balance Dysfunction in Multiple Sclerosis
Stephanie L. Silveira
Robert W. Motl
Francois Bethoux
Introduction
Multiple sclerosis (MS) is a chronic and nontraumatic, disabling disease of the central nervous system (CNS) characterized by axonal demyelination and transection as well as neurodegeneration involving loss of neurons and dendrites.1 There are an estimated 1.1 million people currently living with MS in the United States, and the majority of cases are women of European descent between 20 and 50 years of age.2 The CNS damage in MS is initially the result of immune-mediated demyelination and transection of axons that results in white-matter lesions and later the consequence of insufficient neurotrophic support for maintaining neurons and dendrites within the CNS that results in gray and white matter atrophy.3 The CNS damage, depending on its location, can manifest as a range of symptoms including fatigue, depression, cognitive and visual impairment, muscle weakness, spasticity, and bowel and bladder problems. Another
major consequence of MS is mobility disability, including difficulty with walking, dysfunction of gait, and compromised balance.4 This chapter provides an overview of walking, gait, and balance dysfunction as prominent and life-altering consequences of MS that are important for disease management and rehabilitation by clinicians.
major consequence of MS is mobility disability, including difficulty with walking, dysfunction of gait, and compromised balance.4 This chapter provides an overview of walking, gait, and balance dysfunction as prominent and life-altering consequences of MS that are important for disease management and rehabilitation by clinicians.
Definition of Mobility Disability in MS
We define mobility disability based on problems with walking, gait, and balance that may require the use of an assistive device and interfere with activities of daily living and community integration and participation (i.e., community ambulation). Walking is a form of locomotion (i.e., moving between places) that includes bipedal ambulation across different surfaces, short or long distances, and over or around obstacles.5 Gait is an underlying feature of walking and involves describing the spatial and temporal parameters or characteristics of walking (i.e., the manner in which one walking). Gait is described in part based on step/stride length, cadence, base of support, double-support time, and side-to-side step variability or asymmetry.6 Gait is one of the underlying factors for understanding walking speed, ambulatory endurance, and community ambulation. Balance, defined as maintaining upright stance or posture while standing or moving, can be described by the status or functioning of three sensory systems, namely, visual, somatosensory, and vestibular.1 Balance is important for mobility and walking in MS, as its disruption could result in increased falls or near falls while walking and can certainly be associated with disturbance of gait (e.g., base of support) and walking. These three factors collectively represent major features in the description and understanding of mobility and its disability in MS.
Prevalence of Mobility Disability in MS
Mobility disability is a primary feature associated with the clinical manifestation of MS and its progression over time. This is commonly reported based on Expanded Disability Status Scale (EDSS) scores (i.e., a standardized clinical rating system for MS-related disability)7 in natural history studies of MS, mostly based on the walking distance and the use of mobility aids. These natural history studies have examined the rate or time course and predictors of disability progression in persons with MS based on the time for reaching EDSS scores of 4.0 and 6.0 as benchmarks of irreversible mobility disability. For example, the median times from onset of MS until the assignment of benchmark EDSS scores of 4.0 (i.e., limited walking ability, but able to walk more than 500 m without aid or rest) and 6.0 (i.e., ability to walk with unilateral support no more than 100 m without rest) are approximately 10 and 20 years, respectively.8,9,10 The median
interval of time from the onset of MS until those benchmarks has been predicted by sex, age, symptoms and course at onset of disease, degree of recovery from the first relapse, time to a second neurological episode, and number of relapses in the first 5 years of the disease.8,9,10
interval of time from the onset of MS until those benchmarks has been predicted by sex, age, symptoms and course at onset of disease, degree of recovery from the first relapse, time to a second neurological episode, and number of relapses in the first 5 years of the disease.8,9,10
Population-based studies further indicate that 75% of people with MS report problems with mobility, and difficulty with walking itself is reported by over 40% of people with MS.4,11 Another study of patients with MS in Europe indicated that nearly 50% of people with MS reported experiencing mobility impairments within the first month of diagnosis, and more than 90% of people with MS reported experiencing mobility impairments within 10 years of diagnosis.12 Nearly 70% of people with MS identified walking difficulty as the most challenging part of the disease, and common mobility problems reported by persons with MS included needing to concentrate on walking, difficulty standing, increased effort needed to walk, and needing support such as furniture, walls, or someone’s arm when walking indoors.13 Approximately one-third of people with MS report using at least one mobility device, such as a cane, walker, or wheelchair. Mobility aid use for ambulation is associated with age, worsening health, and secondary progressive MS.13
Balance problems are common among persons with MS and can increase the risk and prevalence of falls as well as decrease physical activity and quality of life (QOL).14,15 Balance problems include increased postural sway during standing, abnormal patterns of movement in static and dynamic balance, and delayed postural reactions.16,17,18 Balance problems typically manifest early in the disease course and worsen over time, with over 50% of persons with MS reporting a loss of balance two or more times weekly.4,19,20 Falls represent a common marker of the presence of balance problems in MS. One prospective cohort study that included persons with MS between 21 and 74 years of age documented the occurrence, over a 6-month period, of three or more falls in 33% of the sample, and between one and two falls in 27%.21 Another study reported a similar fall prevalence in persons with MS who used mobility aids, with 50% reporting 1 or more falls in last 3 months and a range between 1 and 18 falls overall.22 Another study focused specifically on persons with moderate MS-related disability and reported that those who experienced frequent falls (i.e., classified as “fallers”) had more gait dysfunction, including variability in step length and single support.23 This suggests that mobility disability, including balance problems and gait disturbance, is related with falling among persons with MS and is prevalent in a large segment of this population.
Personal Value of Mobility in MS
Mobility is one of the most valued functions among people with MS, as it is critical for independence and its loss increases concern of dependence on caregivers or transition into a nursing home.24 For example,
one national survey of persons with MS reported that 41% of the sample had difficulty walking and 13% were unable to walk at least two times per week.4 Among those who had difficulty walking, 70% reported that it was the most challenging aspect of living with MS.4 The inability and difficulty with walking were rated as the most disruptive problems associated with the management of MS. Furthermore, most people reported at least some adverse impact on one or more everyday activity in the past 6 months because of difficulties maintaining balance (76%). Another study indicated that loss of lower extremity function was rated the highest concern among 13 domains of body function, followed by loss of vision, among persons with MS who had a more recent diagnosis (i.e., less than 5 y) and among those who had a longer time elapsed since diagnosis (i.e., 15 or more years).25 One more recent study had persons with relapsing MS and physicians rate the value of 13 bodily functions from the most to least important using a standard questionnaire.26 Persons with MS rated visual functioning as the primary concern, followed by thinking and memory and walking, whereas physicians rated mobility as the highest concern, followed by thinking and memory.26 Overall, mobility dysfunction is rated as one of the primary concerns among people with MS, and its maintenance is a priority across the disease progression spectrum for both those affected by this disease and their health care providers. These findings are supported by evidence on the burden of mobility disability, as described in the next section.
one national survey of persons with MS reported that 41% of the sample had difficulty walking and 13% were unable to walk at least two times per week.4 Among those who had difficulty walking, 70% reported that it was the most challenging aspect of living with MS.4 The inability and difficulty with walking were rated as the most disruptive problems associated with the management of MS. Furthermore, most people reported at least some adverse impact on one or more everyday activity in the past 6 months because of difficulties maintaining balance (76%). Another study indicated that loss of lower extremity function was rated the highest concern among 13 domains of body function, followed by loss of vision, among persons with MS who had a more recent diagnosis (i.e., less than 5 y) and among those who had a longer time elapsed since diagnosis (i.e., 15 or more years).25 One more recent study had persons with relapsing MS and physicians rate the value of 13 bodily functions from the most to least important using a standard questionnaire.26 Persons with MS rated visual functioning as the primary concern, followed by thinking and memory and walking, whereas physicians rated mobility as the highest concern, followed by thinking and memory.26 Overall, mobility dysfunction is rated as one of the primary concerns among people with MS, and its maintenance is a priority across the disease progression spectrum for both those affected by this disease and their health care providers. These findings are supported by evidence on the burden of mobility disability, as described in the next section.
Burden of Mobility Dysfunction in MS
Mobility disability portends considerable burden for people living with MS. The burden ranges from worsening of symptoms to reduced QOL. Furthermore, there are economic burdens associated with mobility disability as well as influences on participation and employment. The effect of mobility disability even extends into the lives of caregivers. This section provides an overview regarding the effect of mobility on a variety of outcomes in MS.
Fatigue and Depression
Fatigue and depression are two of the most common symptoms of MS, and these two symptoms have been associated with mobility disability in MS. In turn, fatigue and depression further affect community participation and activities. Upward of 95% of persons with MS report fatigue as a burden of the disease that can be severe.27 Fatigue is further a significant predictor of physical functioning and QOL.28,29 One study reported that self-reported fatigue was associated with self-report walking limitations, but it was only mildly associated with objective walking performance tests.30 Additionally,
gait abnormalities analyzed with a body sensor during the 6-minute walk test were associated with higher self-reported overall fatigue impact scores in persons with MS.31 Another study of participants with MS reported that fatigue measured using the Fatigue Severity Scale was significantly associated with the 6-minute walk distance.32 That study also measured self-report depression using the Hospital Anxiety Depression Scale (HADS-D) and reported that the 6-minute walk distance was associated with the HADS-D score.32 Other studies have reported a significant relationship between depression and mobility disability (i.e., gait and balance problems) in MS.33,34 One study demonstrated that persons scoring over 8 on the HADS-D (i.e., elevated depression symptom group) walked slower with a decreased cadence compared with those who had HADS-D scores of 8 or less; depression symptom scores were further correlated with self-perceptions of walking ability.34 Another common measure of depression is the Beck Depression Inventory-II (BDI-II). Depression scores based on the BDI-II were significantly related to both objective and subjective balance scores in a study of ambulatory participants with MS.33 Collectively, mobility disability may be associated with worse fatigue and depression in persons with MS.
gait abnormalities analyzed with a body sensor during the 6-minute walk test were associated with higher self-reported overall fatigue impact scores in persons with MS.31 Another study of participants with MS reported that fatigue measured using the Fatigue Severity Scale was significantly associated with the 6-minute walk distance.32 That study also measured self-report depression using the Hospital Anxiety Depression Scale (HADS-D) and reported that the 6-minute walk distance was associated with the HADS-D score.32 Other studies have reported a significant relationship between depression and mobility disability (i.e., gait and balance problems) in MS.33,34 One study demonstrated that persons scoring over 8 on the HADS-D (i.e., elevated depression symptom group) walked slower with a decreased cadence compared with those who had HADS-D scores of 8 or less; depression symptom scores were further correlated with self-perceptions of walking ability.34 Another common measure of depression is the Beck Depression Inventory-II (BDI-II). Depression scores based on the BDI-II were significantly related to both objective and subjective balance scores in a study of ambulatory participants with MS.33 Collectively, mobility disability may be associated with worse fatigue and depression in persons with MS.
Cognition
There is increasing evidence that mobility disability is associated with cognitive dysfunction in MS (i.e., cognitive-motor coupling). For example, one early study examined the association between motor impairments of the upper and lower extremities and cognitive functioning in MS. That study identified speed of processing and executive function as correlates of upper and lower extremity motor function based on the 9-Hole Peg Test and Timed 25-Foot Walk (T25FW) in persons with MS.35 Another study reported that cognitive processing speed using the Symbol Digit Modalities Test was associated with self-reported and objective walking measures as well as EDSS scores in persons with MS.36 One study of balance using the Six Spot Step Test and cognitive processing speed based on the Paced Auditory Serial Addition test reported an association between balance and cognition.37 These data suggest that persons with MS who have more significant mobility disability have greater cognitive impairments.
There is further evidence of cognitive-motor coupling based on the dual-task paradigm. This paradigm involves examining changes in walking performance or balance (i.e., two metrics of mobility disability) when performing a concurrent cognitive task compared with not performing the cognitive task. One study examined the effect of performing alternate letter alphabet test while walking and reported that the concurrent performance of a cognitive task resulted in significantly slower velocity and cadence, shorter step length, increased step time, and increased double-support
time in persons with MS.38 Other research has demonstrated that balance can be significantly affected while concurrently performing a cognitive task in persons with MS. For example, one study of balance using the dual-task paradigm in persons with both mild and moderate MS reported that postural sway measured using posturography was significantly increased when completing a word generation task, and the change was significant across disease severity levels.39 These data provide a direct link between cognitive functioning and walking and balance function in MS.
time in persons with MS.38 Other research has demonstrated that balance can be significantly affected while concurrently performing a cognitive task in persons with MS. For example, one study of balance using the dual-task paradigm in persons with both mild and moderate MS reported that postural sway measured using posturography was significantly increased when completing a word generation task, and the change was significant across disease severity levels.39 These data provide a direct link between cognitive functioning and walking and balance function in MS.
Quality of Life
QOL is defined as the subjective evaluation or judgment regarding satisfaction with life and can be directly influenced by mobility disability. One study of 103 patients with MS reported that QOL, rated using the Multiple Sclerosis Quality of Life-54, was significantly associated with disability level, depression, and fatigue.40 Another study reported that persons with MS scored significantly lower than controls on the Quality of Life Index (QLI), and the degree of disability measured by EDSS scores was predictive of QLI score.41 Health-related quality of life (HRQOL) has further been examined as a correlate of walking dysfunction in persons with MS. One retrospective study of three clinical trials of patients with MS reported that HRQOL measured using the SF-36 was significantly correlated with walking speed, with participants with faster speed reporting higher SF-36 physical component scores. That study further examined the association between longitudinal changes in SF-36 scores and walking speed over time and reported that participants with MS whose walking speed decreased had decreased SF-36 scores; these changes in both SF-36 scores and walking speed were in the clinically significant range, with a 20% to 25% decrease in walking speed being associated with a five-point decrease in SF-36 physical component score.42 Other research has reported that impaired balance and coordination is among one of the common problems associated with diminished QOL of persons with MS.43 This collectively suggests that disability severity and mobility disability are associated with worse QOL and HRQOL in persons with MS.
Economic Burden
The economic burden of MS can be understood, in part, based on the association between EDSS scores and costs of the disease. Costs associated with MS include medications and hospitalization as well as other direct costs, indirect costs, informal costs, and intangible costs.44 Reviews of the literature report a stark increase in disease-related costs with increasing EDSS scores (i.e., overall mobility disability) in persons with MS.44,45 In one study, those with mild MS (EDSS <3) incurred approximately $16,646
in annual disease-related costs, compared with $27,151 in those with moderate disease (EDSS 3-6), and even higher costs were presumed for those with severe disability (EDSS >6).46 One study of health care-related costs for persons with MS reported that the average annual cost for medical care in persons with abnormal gait was $20,871.47 Disease-modifying drugs (DMDs) are more often prescribed to those with abnormality in gait, and the average additional cost associated with DMDs in persons with MS is $7901 annually.47 Overall, patients with walking impairment are more likely to need a variety of expert medical services outside of primary care and long-term DMD treatments that can contribute to the economic burden of MS disease management.48
in annual disease-related costs, compared with $27,151 in those with moderate disease (EDSS 3-6), and even higher costs were presumed for those with severe disability (EDSS >6).46 One study of health care-related costs for persons with MS reported that the average annual cost for medical care in persons with abnormal gait was $20,871.47 Disease-modifying drugs (DMDs) are more often prescribed to those with abnormality in gait, and the average additional cost associated with DMDs in persons with MS is $7901 annually.47 Overall, patients with walking impairment are more likely to need a variety of expert medical services outside of primary care and long-term DMD treatments that can contribute to the economic burden of MS disease management.48
Participation/Employment
Participation is defined as involvement in a life situation,5 and employment is one of the primary determinants or indicators of participation. Mobility disability is associated with early retirement and work absences that significantly affect income in this population.49 For example, an estimated $17,000 annually per patient is lost in relapse-related absences, reduced time spent at work, and early retirement.49 North American Research Committee on Multiple Sclerosis (NARCOMS) patient registry data demonstrate that, on average, over 50% of patients with MS are not employed and those who are unemployed are more likely to have progressive disease, longer symptom duration, greater levels of disability, and greater functional limitations.50 Furthermore, mobility performance subscale scores of the performance scales were predictive of work loss and work initiation longitudinally, with increased mobility problems predictive of loss and reduced mobility problems predictive of initiation.50 Another study reported that only 34% of people who report walking difficulty were employed.4 Objective measures of walking, including the T25FW, and self-report measures, such as the 12-item Multiple Sclerosis Walking Scale (MSWS-12), have been used to measure the association between mobility disability and employment.51,52 For example, one study reported that longer T25FW times were associated with permanent disability (collecting Supplemental Security Income), government health care assistance (Medicaid/Medicare), and change in occupational status.51 Issues with mobility and the subsequent impact on participation, particularly employment status, can affect feelings of independence in patients with MS.
Independence
Independence is defined as having choice and control over life and your environment and is directly associated with the presence and degree of mobility disability in MS. The need for assistance in activities of daily
living further contributes to feelings of loss of independence and burden in persons with MS.24 One study reported that approximately two-thirds of people with MS were dependent on a caregiver for assistance in activities of daily living, specifically mobility-related activities, such as walking outside, negotiating stairs, and navigating to social and lifestyle activities.24 In studies using both objective and self-reported measures of walking disability, participants with greater disability severity reported a greater need for assistance with instrumental activities of daily living, such as preparing meals and managing medications.51,52 In another study examining T25FW performance, participants who took longer than 8 s to complete the task had more difficulties in performing instrumental activities of daily living.51 Balance problems associated with MS can further affect independence as suggested in one study reporting that persons with MS demonstrated significant postural challenges when performing movements involved in execution of activities of daily living, particularly during head, hand, and dynamic movements.53 Overall, activities that seem to be most affected by MS are mobility related and include walking outside, cleaning indoors, negotiating stairs, dressing, outdoor transportation, and social and lifestyle activities.54 Factors related to mobility disability and decreased independence are interrelated with employment and economic burden of MS, themselves closely related to dependence on caregivers.
living further contributes to feelings of loss of independence and burden in persons with MS.24 One study reported that approximately two-thirds of people with MS were dependent on a caregiver for assistance in activities of daily living, specifically mobility-related activities, such as walking outside, negotiating stairs, and navigating to social and lifestyle activities.24 In studies using both objective and self-reported measures of walking disability, participants with greater disability severity reported a greater need for assistance with instrumental activities of daily living, such as preparing meals and managing medications.51,52 In another study examining T25FW performance, participants who took longer than 8 s to complete the task had more difficulties in performing instrumental activities of daily living.51 Balance problems associated with MS can further affect independence as suggested in one study reporting that persons with MS demonstrated significant postural challenges when performing movements involved in execution of activities of daily living, particularly during head, hand, and dynamic movements.53 Overall, activities that seem to be most affected by MS are mobility related and include walking outside, cleaning indoors, negotiating stairs, dressing, outdoor transportation, and social and lifestyle activities.54 Factors related to mobility disability and decreased independence are interrelated with employment and economic burden of MS, themselves closely related to dependence on caregivers.
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