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Aging With a Progressive Neurologic Disease

Rehabilitation Management of the Adult Aging With Parkinson Disease or Multiple Sclerosis

Karpatkin, Herb DSc, PT, NCS, MSCS; Cohen, Evan PhD, MA, PT, NCS

doi: 10.1097/TGR.0000000000000232
Aging With a Progressive Neurologic Disease
Free

The confluence of an aging population and increasing life expectancy of people with neurodegenerative diseases such as Parkinson disease and multiple sclerosis means that there is a growing segment of the population who are aging with a neurodegenerative disease. As such, rehabilitation professionals must be prepared for the combined challenges of age- and disease-related changes in physical function. First, a review of age- and disease-related problems experienced by older adults with Parkinson disease or multiple sclerosis will be presented, followed by a description of clinical practices that might be implemented by rehabilitation professionals to best address the problems experienced by these unique populations.

Physical Therapy Program, Hunter College—City University of New York, New York (Dr Karpatkin); and Physical Therapy Program—South, Rutgers, The State University of New Jersey—School of Health Professions, Blackwood (Dr Cohen).

Correspondence: Evan Cohen, PhD, MA, PT, NCS, Physical Therapy Program—South, Rutgers, The State University of New Jersey—School of Health Professions, 200 College Dr, PO Box 200, Jefferson Hall, Ste 308, Blackwood, NJ 08012 (cohenet@shp.rutgers.edu).

The authors have disclosed that they have no significant relationships with, or financial interest in, any commercial companies pertaining to this article.

Degenerative diseases present a special challenge to clinicians, as they are by definition, conditions that can worsen over time despite best practices by the health care team. As medical management for persons with progressive neurologic conditions improves, patients with these diseases are living for longer periods of time. A result of this is the new diagnostic challenge for practitioners: the patient aging with a progressive neurologic condition. As adult aging is essentially a process of diminishing function of various body structures and functions, it also can be looked at as a progressive condition. The older adult with a neurodegenerative disease therefore will present with 2 separate and interacting progressive conditions. The purpose of this article is to examine the issues relating to physical therapy management of patients aging with Parkinson disease (PD) and multiple sclerosis (MS), 2 diagnoses commonly faced by rehabilitation clinicians. Although both PD and MS are progressive central nervous system (CNS) conditions, they each have separate and distinct clinical characteristics and, as a result, different interactions with the complications that occur as a result of aging.

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AGING AND PD

Parkinson disease is one of the most common neurologic diseases worldwide with an estimated incidence of 4.5 to 21 cases per 100 000 population per year and prevalence ranging from 18 to 328 cases per 100 000 population.1 It is also conspicuously associated with aging, with 60 years of age being the most common age of onset with diagnosis before the age of 40 years being uncommon. It affects 1% of all individuals above the age of 60 years.1 As a person ages, the risk of developing PD escalates as cell loss increases in the substantia nigra at a rate of 4.7% to 9.8% every decade. Even older adults without PD symptoms show evidence of substantia nigra cell loss.2,3 In contrast, other areas of the brain are less susceptible to age-related deterioration. Areas such the hippocampus, putamen, medial mammillary nucleus, hypothalamus, and the nucleus basalis of Meynert remain relatively stable during aging, while neocortical neurons might show a loss of only 10% over the life span.4 This information establishes that PD is clearly associated with aging. As the numbers of our aging population increase, we should expect a concomitant increase in numbers of persons with PD. As some of the cardinal signs of PD relate to poorer movement, clinicians who specialize in movement, such as physical and occupational therapists, must play a major role in their care. Because of the relationship between PD and aging, therapists must be mindful of the fact that problems seen in this population may be related to PD, age-related changes, or the combined effect of both. The effects of aging on mobility should be looked at as an interaction of multiple conditions, each resulting in unique and specific issues requiring unique and specific interventions. When these movement issues are combined with those resulting from PD, a distinct clinical picture emerges with which clinicians must be familiar to provide optimal care. The purpose of this section is to provide an in-depth description of the patient with both PD and age-related changes and to present a clinical framework for examination and intervention for such patients.

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Aging and PD—separate contributions to mobility loss

Healthy older adults and persons with PD have many similarities that may lead a clinician to think that PD and aging are synonymous. This is especially true in the area of balance and falls. Both persons with PD and healthy older adults have diminished postural control and a resulting increased likelihood of falls. This suggests that a similar deterioration of neural mechanisms mediating balance occurs in both populations. However, the evidence suggests that diminished postural control in older adults differs from what is seen in PD. In a review article comparing postural control changes in the older adults with those seen in people with PD, Romero and Stelmach5 described the following findings:

  1. Older adults have increased postural sway in static standing compared with younger adults, while in PD postural sway can be either increased or decreased.
  2. Older adults present with increased postural sway when sensory information is limited. Diminished visual, somatic, and vestibular sensation coupled with poorer sensory processing is common in older adults. Because of the losses across sensory modalities, older adults have little ability to compensate for the loss. In contrast, persons with PD have a decreased ability to utilize their intact sensory apparatus to adapt to changing sensory conditions. In other words, older adults have difficulty with balance due to a loss of sensory modalities, while persons with PD may have the appropriate sensory modalities but are unable to access them for use.
  3. In response to perturbations, older adults tend to show impaired timing and amplitude between synergistic muscles used to maintain stability, for example, using a hip strategy when an ankle strategy is appropriate. Older adults also exhibit prolonged onset and insufficient amplitude of postural responses when their balance is perturbed. In contrast, persons with PD show reduced amplitude of long latency reflexes and increased amplitude of medium latency reflexes.

Romero and Stelmach5 suggest that balance and falls in older persons with PD therefore represent a combination of both age- and disease-related factors. It may also be the case that some of the age-related changes are due to disuse and a sedentary lifestyle. As such, they may be remediable by therapy that focused on reconditioning. The clinical implication is that multiple reasons for balance loss of differing etiologies may coexist in older people with PD. This suggests that clinicians working with this population will need to evaluate for multiple potential areas of balance loss to construct an appropriate intervention plan.

Further underscoring the difference between older adult fallers with and without PD is a study by Weaver et al6 who used videotape analysis of falls in both groups in a long-term care facility, giving “real world” observations regarding what leads to falls in older adults. The primary difference between groups was that persons with PD were 1.3 times more likely to fall as a result of difficulties with proper weight shifting; falls were more likely to occur during tasks such as turning, transitioning from sit to stand, and bending forward. Similarly, it was found that when a loss of balance did occur, people with PD were more likely to react by reaching for an external support surface while those without PD would react with a weight shift or a stepping strategy.

The similarities in loss of postural control between older adults with and without PD have led some to consider PD as a form of accelerated aging.7 However, it is more likely that the postural control issues associated with aging interact with those seen in PD, resulting in a worsening of overall disability. Although research has established differences between the postural control limitations caused by aging and by PD, the interaction effect of age- and PD-related changes is not clear.

Levy8 proposed that the following issues would be prominent in older people with PD: first, patients with onset of PD symptoms at an older age tend to show a faster rate of disease progression. Second, older adults with PD have diminished responsiveness to dopamine therapy than younger ones. In particular, gait and balance are less responsive to dopamine therapy in middle and late stages of PD, while symptoms such as tremor, rigidity, and bradykinesia respond to dopamine replacement over the course of the disease. This may suggest that some of the gait and balance loss seen in older adults with PD is not related to the disease but to other factors that may be ameliorable with rehabilitation interventions. Third, older age at the time of diagnosis is also associated with worsening cognitive impairment and onset of dementia.

This suggests the possibility that advanced age at the time of PD diagnosis may be a more important indicator of clinical impairment than years since diagnosis. The clinical picture of the older adult with PD, therefore, seems to be an interaction of damage to dopaminergic structures resulting in tremor, rigidity and bradykinesia, and nondopaminergic, subcortical structures leading to axial impairment such as difficulties with gait and balance. This does not rule out the contribution of PD to axial impairment, but that the predominant contribution may be due to advancing age rather than disease severity.

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Musculoskeletal changes in older adults

Many of the orthopedic changes that are seen in persons with PD that contribute to loss of postural control may be associated with aging.9 Loss of flexibility in the ankle plantarflexors combined with weakness in the dorsiflexors leads to more difficulty with achieving a heel initial contact and increases the likelihood of catching the toe when walking on an uneven surface, which may lead to a fall. This type of gait is similar to the shuffling seen in persons with PD but is due to orthopedic rather than neurologic causes and therefore would likely be amenable to physical therapy intervention. Gait in older adults has been described as “broad-based, with small steps, diminished arm swing, stooped posture, flexion of the hips and knees, uncertainty and stiffness in turning,”10 a description that certainly would apply to gait of people with PD.

Similarly, excessive thoracic kyphosis common in the older adults due to prolonged sitting in a stooped posture or compression fractures in the spine can mimic the flexor-bound posture that is seen in people with PD. Although in both conditions the goal would be to resume normal upright posture, excessive spinal flexion in older adults is more apt to be due to soft tissue shortening and loss of vertebral body height as well as other orthopedic changes, while in people with PD neurologic causes such as anteropulsion or truncal dystonia may be responsible. Abe et al11 suggested that that the predominant reason for trunk flexion in PD may be predominantly orthopedic in nature, but the influence of neural contributions needs to be considered.

Diminished hip extension is another common finding in both older adults and persons with PD.12 During the stance phase of gait, the hip does extend to neutral and hip extension force is decreased, resulting in impaired gait stability and a shortened stride length. It can be presumed that the lack of hip extension commonly found in older adults is due to orthopedic changes or to a compensatory gait pattern adopted to minimize stride length. In persons with PD, the lack of hip extension may be due to rigidity, bradykinesia, or dystonia, as well as compensatory processes to minimize instability. The fact that this and other gait impairments improve with administration of levodopa suggests that gait changes in older adults with PD represent a combination of PD-related neurologic factors and orthopedic factors specific to aging. Therefore intervention on the level of orthopedic impairment may not result in improvements due to persisting neurologic involvement.

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The role of fatigue in aging and PD

Fatigue is a common finding in both older adults and persons with PD13 and can lead to falls and worsen postural control. There are both separate and similar components to the fatigue found in each group. Clinicians working with these populations must therefore be aware of how fatigue can affect performance in each case.

Although PD-related fatigue has been found to have both mental and physical components, these 2 types of fatigue do not correlate suggesting that the 2 are somewhat independent.14 It has also been found that persons with PD use more energy than normal controls both at rest and during motor tasks, but no differences were found in energy efficiency between fatigued and nonfatigued PD populations. This suggests that people with PD were not fatigued simply because they worked harder, but that the fatigue was a distinctive physiologic process in persons with PD.15 In contrast, fatigue in older adults is multifactorial, potentially involving muscle breakdown, disuse atrophy, difficulties in oxygen transport, cardiac inefficiency, depression, sleep disorders, polypharmacy, and increased physiological costs due to the use of inefficient movement patterns.16

Clinicians working with the older adults with PD should be aware that fatigue can be a predisposing factor to falls and therefore be prepared to evaluate for its presence. Many of the causes of fatigue in this population may be secondary rather than primary and therefore more ameliorable to treatment intervention.

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A framework for physical therapy examination of the older patient with PD

The older adult with PD presents a challenge for the clinician as the problems with body structure/function and activity can be from overlapping sources. As previously presented, loss of mobility in older adults with PD can result from issues related to the PD pathology, from age-related changes, or an interaction between the 2. Further complicating the picture is that some of the issues may be primary to one of the diagnoses (ie, problems that arise directly from the health condition or pathology), but many of the findings may be a result of secondary issues (ie, consequences that arise from the primary that occur over time after the onset of the condition or pathology), related to lifestyle changes that were adapted because of the course of the disease. A list of possible findings of each pathology can be found in the Table.

TABLE

TABLE

The picture that emerges of the older person with PD is that of an individual dealing with 2 distinct but interacting disease states. It is important for the clinician to be aware that these are separate phenomena occurring in the same patient, and that aging is not necessarily part of PD, nor is PD part of aging. However, when both occur in the same individual, the clinician's responsibility is to be able to examine and evaluate for signs and symptoms of each condition and develop treatment interventions for each.

In evaluating the older person with PD, the clinician should be aware of the following possible findings:

  • In static standing, postural sway can be increased or decreased.
  • If sensory testing reveals loss of sensory modalities, this is more likely to be due to aging. If sensory modalities are intact, but there is evidence of their not being utilized, this suggests that loss of balance is more likely to be due to PD.
  • If a perturbation that causes a loss of balance results in the patient reaching for a support surface, this suggests parkinsonian influences. If, however, the loss of balance leads to the use of ankle, hip, or stepping strategies, this is indicative that the balance loss was more likely due to aging.
  • If the patient presents with a trunk-flexed posture that does not correct with stretching of shortened flexors or strengthening of overstretched extensors, this suggests that the posture may be a result of PD-related problems such as dystonia or anteropulsion
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Intervention strategies

Physical therapy intervention for the older adult with PD is complex. Although no specific evidence-based studies have been performed, the following recommendations can be made for addressing the problems with body structure/function and activity limitations noted previously.

Balance and functional mobility training should be of the highest priority for the older adult with PD. Difficulties in static standing can be detected by having the patient stand comfortably but also under alternate conditions including different limb positions (eg, narrow base of support, tandem standing, and single limb stance) and with eyes open or closed. The task of static standing can be made more complex by altering the support surface or by giving competing attentional tasks. In any of these cases, the task requires that person maintain stability in the presence of multiple destabilizing forces.

Intervention should start with finding a position that the individual can maintain with stability. Using visual feedback by having the patient maintain visual fixation on a stable object may help with this. Once the individual can maintain a stable static position, add complexity to the task by changing foot position, closing the eyes, changing the support position, or giving a dual task. Examples of changing foot position could include placing the feet progressively closer together, placing the feet in tandem or semitandem stance, or even standing on a single limb. Use a variety of different foot positions to discover which are the most challenging and to expose the individual to as wide an array of different static standing conditions as possible. This will help them develop a wider repertoire of situations under which they will be able to successfully meet the needs of tasks that require stable static standing positions. Performing these activities with eyes closed requires that the individual use other sensory modalities besides vision, which may be helpful if these sensory modalities have become inactive as a result of lack of use. Examples of altered support conditions include having the patient stand on more compliant surfaces such as a thick rug or foam, on uneven terrain where the feet are at different heights, or at different grades of inclination. Practicing these tasks under different attentional demands will add another layer of complexity as dual-task performance has been found to be limited in both older adults and in people with PD. Examples of dual tasks might include having the person maintain static standing while performing mentally challenging calculations (counting backward by 7's), describing a scene or situation, or even carrying on a conversation. Alternatively, having the person perform static standing tasks in a busy environment where the attentional demands are greater will add similar “real-world” stimulation to the activity.

The use of large amplitude training, such as the LSVT BIG program, is a relatively new approach to treating the bradykinesia common in persons with PD, and there is some useful evidence of its effectiveness.17,18 However, the use of this intervention in older adults with PD may be somewhat problematic, as the high velocity and range that the movements of large amplitude training require may cause damage to the musculoskeletal system. These techniques should be utilized with a degree of caution in frail older adults with PD, perhaps starting with smaller and slower movements than what might be tried with a younger person with PD.

Underlying impairments such as restricted range of motion or strength in the lower extremities or trunk can be addressed with stretching or strengthening protocols. If the evaluation reveals sensory loss as an impairment leading to balance loss, then training the individual to compensate using intact sensory modalities can be attempted. If, however, sensation appears to be intact, and the problem appears to be lack of use of intact sensory modalities, placing the patient in situations where specific sensory modalities are required (eg, balancing with eyes closed to force the use of underutilized somatosensory skills) can be tried.

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AGING AND MS

Multiple sclerosis is a progressive autoimmune disease that causes demyelination of axons in the CNS. Any CNS structure can be affected, resulting in a disease process that can be extremely variable in presentation and prognosis. This represents a challenge for clinicians working with persons with MS as, unlike other neurologic conditions, there is no stereotypical presentation upon which to base a framework of examination, evaluation, and intervention. The interaction of a highly variable presentation and a progressive course adds to the difficulty that clinicians face.

Recent improvements in medical management of MS have resulted in reduced overall disability and disease progression. This has led to an increase in the life span of persons with MS. The average age of persons with MS is rising. The number of persons with MS older than 65 years has increased, presumably as a result of better medical management.19 As a result, there is a growing number of older persons with MS who require the assistance of physical therapists to optimize their mobility.

The aging patient with MS should be considered a distinct diagnostic entity as it represents the interaction of 2 specific groups: the older adult patient and the MS patient, each with discrete findings and indications for examination, evaluation, and treatment. Further adding to this complexity is that both aging and MS represent progressive conditions, where multiple systems can be affected in different ways.

The purpose of this section is to present the information about the person aging with MS so that clinicians who work with this population can have a clearer picture of likely challenges. The primary questions to be answered are as follows: (1) How does advancing age affect the MS disease process? (2) How do MS symptoms interact with the aging process? Following this, a framework for evaluation and treatment will be presented.

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Influence of aging on the course of MS

Multiple sclerosis is a progressive condition, with accumulation of deficits typically occurring over years. Because of its variable nature, the progression of MS over a lifetime can be specific to certain regions of the CNS or present in new and different ways and locations over time. Aging can also be considered a progressive condition, characterized by loss of various functions over time, each potentially resulting in loss of function.

Although relapsing-remitting MS (RRMS) is the most common disease phenotype, persons older than 65 years with MS are more likely to be diagnosed with a progressive form of the disease. If the diagnosis of MS occurs past the age of 65 years, it is more likely to be primary progressive MS; if the person was diagnosed at a younger age, he or she is more likely to have converted from RRMS to secondary progressive MS.20 This may suggest that aging increases the risk of conversion from RRMS to a more progressive form of the disease. Although older age at disease onset (ie, late-onset MS) is relatively rare, it is associated with a progressive disease course, earlier progression from RRMS to secondary progressive MS, and an earlier onset of disability.

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Effects of aging on MS neuropathology

Multiple sclerosis is a disease of progressive neuropathology, which is largely a result of CNS tissue loss. However, progressive tissue loss also occurs in the aging population. Brain volume decreases by 0.7% to 1.0% per year in persons with MS and decreases by 0.01% to 03% in healthy older adults.20 This indicates that in the aging MS patient, there is a cumulative effect of both aging and MS disease processes leading to CNS tissue loss that is greater than the individual effects of each. The aging person with MS therefore faces a greater loss of CNS tissue, which may reflect greater disability than each condition individually.

A significant amount of the recovery from the effects of MS progression, whether as a result of relapses or progressive disease, is mediated by oligodendrocytes. Oligodendrocytes are the cells that are responsible for the production of CNS myelin. In older persons with MS, this recovery is limited due to an age-related decrease in the production of oligodendrocytes.21 This results in a decreased ability to remyelinate CNS axons as a response to disease activity and the diminished ability to recover functional abilities lost as a result. Older adults with MS are therefore more limited in their ability to recover from MS progression due to a failure of an underlying physiologic mechanism that is intact in younger persons with MS. Interestingly, the age-related reduction in remyelination occurs at approximately the same age when the disease often evolves from RRMS to secondary progressive MS, suggesting that aging may be in some ways related to this transition.22 If disease behavior may be tied to age, then interventions that have been shown to slow some of the processes associated with aging may have a place in limiting MS disease progression.

Although MS is well known to be an autoimmune disease, abnormal immunologic responses are responsible for many age-related conditions including types of cancer, cardiovascular disease, and increased susceptibility to both viral and bacterial infections. The already altered immune response in persons with MS may cause these types of conditions to occur at earlier ages than in those without MS.23 In this way, it may be the case that persons with MS experience the deficits associated with aging earlier than in persons without the disease.

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Comorbidities of aging and MS

It is difficult to determine whether the worsening symptoms seen in older persons with MS are due to the aging process, the MS disease process, or some interaction between the 2. Many issues of impaired mobility and cognition commonly seen in one condition could be seen in the other. In addition, certain neuropathologic diseases are common in older adults (eg, PD or Alzheimer disease) and could be mistaken for MS findings when in fact they represent separate and distinct disease processes. The question of whether the deficits seen in older adults with MS are a result of aging or the MS disease process is important for clinicians working with this population, as different physical therapy interventions might be needed for each respective condition.

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Vascular comorbidities

Vascular comorbidities such as hypertension, peripheral vascular disease, and heart disease are common in older adults. In older persons with MS, they can impair walking ability by decreasing the individual's ability to engage in exercise and mobility tasks.24 The presence of these vascular comorbidities can shorten the time from diagnosis to significant mobility disability.

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Impaired mobility

Multiple sclerosis is predominantly a disease of mobility. Although the underlying physiologic substrate is autoimmune-mediated CNS demyelination, the result is a diminished ability to use one's body to achieve task goals. Similarly, aging is well known to affect mobility. Multiple impairments associated with aging result in diminished function of the musculoskeletal and neuromuscular systems, making movement more difficult. The combination of both is likely to lead to a notable loss of the ability to move normally. Not surprisingly, older persons with MS have more movement-related disability than their healthy age-matched peers.25 Older persons with MS are more likely to use an assistive device such as a cane, crutches, walker, or brace for ambulation, or required a wheelchair or scooter.26 These difficulties with mobility invariably result in worsening of health-related quality of life, as they lead to difficulty living independently or leaving the home without assistance.

Falls are a common finding in both older adults and persons with MS and carry with them a great risk for morbidity and mortality.27 Fall-related injuries such as hip fractures and head trauma can be the sentinel event that results in prolonged and costly periods of hospitalization and long-term care. The use of assistive devices is commonly thought to decrease the likelihood of falls. However, the use of assistive devices is not without its limitations.28 Use of an assistive device such as a cane, crutch, or walker prevents the individual from assuming a normal gait pattern. Step lengths can become unequal, arm swing becomes asymmetrical or lost entirely, and the ability to use the upper extremities for balance or to hold other objects is lost. Use of a wheelchair as a primary means of mobility may decrease the risk of falls that occur as a result of walking, but the decrease in the amount of walking likely will lead to a worsening of weakness as a result of disuse. Prolonged sitting may result in loss of flexibility in the lower extremities and trunk. The decrease in aerobic exercise in a population that is already deconditioned can increase the possibility of cardiorespiratory issues. Even the use of a brace such as an ankle foot orthosis (AFO) to aid in decreasing foot drop or foot drag that can result in loss of balance and falls may have negative consequences. The use of an AFO immobilizes the foot, which leads to decreased strength and flexibility. In addition, the use of an AFO alters walking biomechanics throughout the limb and trunk, which may result in unintended, negative consequences. This is not to say that assistive devices should not be considered, but rather the use of physical therapy to help the individual to regain the strength, flexibility, and skill needed to perform mobility tasks should be considered before giving a compensatory device.

Weakness is a common finding in persons with MS. It can be primary, due to corticospinal tract involvement, or secondary, resulting from deconditioning and disuse atrophy.29 Weakness in healthy older adults is more likely to be due to age-related changes in lower motor neuron function although deconditioning and disuse atrophy can also play a major role30 To delineate between weakness due to CNS involvement and weakness due to deconditioning, it will be useful to evaluate for the presence or absence of upper motor neuron findings such as spasticity, hyperreflexia, and pathologic reflexes (eg, clonus and Babinski). To determine whether weakness is due to deconditioning and disuse, a history reflecting a sedentary lifestyle can be informative. If weakness resolves quickly with a basic conditioning program, that is an indication that it was not due to overt pathology. Lower motor neuron conditions that can lead to weakness in older adults include cervical or lumbar spondylolisthesis, and peripheral nerve lesions, which lead to problems such as diminished deep tendon reflexes and disuse atrophy.31

Changes in sensation are a common finding in people with MS.32 Because of the variable nature of the disease, sensory changes in persons with MS can take many forms, including paresthesias, dysesthesias, and impaired perception of temperature. Pain is a common primary sensory finding in MS; however, it may also be secondary due to spasticity, or orthopedic problems caused by poor posture or the use of inappropriate movement patterns.33 Sensory abnormalities are also common in the older adults but are more often due to peripheral rather than central sensory dysfunction. Secondary causes of pain or sensory abnormalities in the older adults can be similar to those seen in those with MS, resulting from orthopedic rather than neurologic abnormalities.34 The presence of pain being accompanied by lower motor neuron signs suggests that the pain is not due to MS. Pain or sensory syndromes worsening with heat, fatigue, or stress are more suggestive of their being due to MS.

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Fatigue

Fatigue is one of the most common complaints reported by persons with MS and can result from factors directly due to the disease as well as secondary factors such as deconditioning, sleep disturbance, and depression.35 It can have a direct effect on mobility, decreasing the ability to participate in exercise programs and physical therapy in general, leading to a vicious cycle of fatigue, inactivity, and deconditioning. In older adults, fatigue is also a frequent problem, occurring as a result of many of the common comorbidities associated with aging such as infection, cancer, anemia, sleep disturbance, orthopedic problems, polypharmacy, and cardiopulmonary dysfunction.13 Similar to MS, all of these can result in deconditioning, which can worsen fatigue and lead to a similar cycle. In both cases, addressing the deconditioning through a judicious exercise program can limit the effects of the fatigue. Where possible, addressing as many of the secondary causes of the fatigue medically can further limit its overall limiting effects.

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Heat intolerance

Heat intolerance is a common complaint of persons with MS. It not only prevents persons with MS from tolerating warmer weather but also more importantly limits their ability to participate in exercise programs as exercise can increase core temperature.36 Older adults also have difficulty with tolerating heat as a result of loss of homeostatic mechanisms and diminished autonomic function.37 This can diminish their ability to participate in exercise programs, limiting their ability to address mobility problems. Older adults with MS therefore present with greater issues of heat intolerance than persons with either diagnosis.

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Behavior and cognition

Multiple sclerosis can affect all parts of the CNS, including cortical areas. As result, impairments in behavior and cognition can occur. Depression, both primary and reactive, is a frequent finding in people with MS, occurring 3 times more frequently than in people without MS, and the suicide rate in persons with MS is 7.5% higher than in people without MS.38 Depression is also a common finding in older adults, but it is more likely to be reactive when compared with MS.39 In older adults with MS, depression is therefore a very likely finding and its effect can impact participation in physical therapy and exercise programs. Interestingly, there is no increase in anxiety for older adults with MS.40

Cognitive impairment is a relatively common finding in people with MS with slowed cognitive processes and deficits with episodic memory reported most frequently.41 Worsening of language, rapid forgetting, and dysnomia are generally not associated with MS; therefore, older adults who present with these symptoms are more likely to be showing the effects of a dementing process such as Alzheimer disease or multiinfarct dementia.42 Generally speaking, there are fewer reports of cognitive and behavioral problems in older than in younger persons with MS. Although part of the reason for this may be an issue with self-reporting or a lack of valid and reliable outcome measures, it may also be the case that older persons with MS are better able to cope with disability than younger persons do. Reasons for this may reflect the following:

Pacing: Older persons with MS have learned how to pace themselves so that they are able to parcel out their energy over the course of the day, allowing them to accomplish more with less fatigue.43

Planning: Older persons with MS are more likely to plan activities that take their MS deficits into account, such as investigating options for accessibility and mobility. It may be that older persons with MS have benefitted from their age and experience so that they are able to better plan and pace their days to accomplish the greatest amount with the least amount of work. Similarly, older persons with MS were better able to determine their own needs, giving them greater life satisfaction and senses of well-being.44

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Medication

One of the primary reasons that mobility has increased in persons with MS over the last 10 to 20 years is large improvements in medical management of the disease. The use of disease modifying therapy (DMT) has resulted in a notable decrease in the frequency and severity of MS relapses. Similarly, earlier diagnosis has resulted in earlier administration of DMT over the course of the disease, resulting in a slower accumulation of disability.

Older persons with MS more frequently have a progressive form of the disease rather than RRMS. Since the indication for the use of DMTs in progressive disease is limited, older people with MS are usually less likely to be receiving DMT.45

Older people with MS have other issues related to medication. The rate of medication clearance is slower in the older adults.46 Medications commonly used to treat spasticity and sensory symptoms in MS such as baclofen and gabapentin can lead to lethargy and sedation as a result of diminished drug clearance. This can result in physicians prescribing less than optimal doses of these medications to older patients with MS leading to incomplete management of these symptoms.

Another issue related to medication in the older persons with MS is that of polypharmacy. Persons with MS often take a great many medications to both modify the disease and treat the associated symptoms.47 Older adults often are heavily medicated to address the multiple comorbidities associated with the aging process. The individual as well as interactive effects of multiple medications can cause an increase in fatigue and worsening of cognition and mood, as well as lethargy and drowsiness, all of which can be mistaken for symptoms of MS. For this reason, physicians should carefully monitor medications in this population.

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A framework for evaluation and intervention for older adults with MS

The older adult with MS presents a challenge for the clinician who wants to improve his or her mobility skills. The combination of the primary and secondary aspects of MS, the comorbidities associated with aging, and the progressive nature of both conditions necessitate the use of careful examination and evaluation so that an appropriate intervention strategy can be developed. Although the multifactorial nature of the problems experienced by the aging MS patient prevents the possibility of providing a complete guide for clinical work, focusing on the following areas can assist with developing a viable examination and evaluation strategy.

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Fatigue

Fatigue is one of the most common problems experienced by people with MS. Its primary and secondary effects on mobility are of particular importance to physical therapists as its presence can limit the ability to participate in mobility activities and will lead to a more rapid decrease of ambulation and balance function. More importantly, the presence of fatigue can limit or prevent the persons with MS from participating in exercise and physical therapy activities at a high enough volume to lead to lasting change. Simply, fatigue can limit or prevent the persons with MS from exercising, and exercise is needed to address the mobility loss that is ubiquitous in MS.

Multiple sclerosis fatigue is multifactorial, with both primary and secondary characteristics. Primary fatigue can be characterized by motor fatigue, which presents as a progressive worsening in an ability to perform a motor task over time, and lassitude, which presents as a more global fatigue that is experienced regardless of activity level. Secondary fatigue occurs as a result of factors that are not immediately related to disease activity. Although secondary fatigue in MS can be due to infection, sleep disorder, pain, and depression, what is of most importance to clinicians working with the population is that secondary fatigue can occur as a result of disuse; fatigue in MS can be largely due to the fact that persons with MS adopt less active lifestyles resulting in a worsening cycle of inactivity and deconditioning. Addressing the deconditioning with exercise programs can often be of limited use as the fatigue itself prevents exercise from being performed at a high enough volume to significantly impact the deconditioning. Fatigue in older adults is also common but is more likely to be the result of cardiopulmonary, orthopedic, or systemic comorbidities associated with aging. These comorbidities can lead to a progressively sedentary lifestyle, resulting in a similar cycle of inactivity, deconditioning, and increasing fatigue for mobility. The picture that emerges of the older MS patient is one with both primary fatigue due to the MS and multifactorial secondary fatigue due to the secondary effects and comorbidities associated with the 2 conditions. Thus, the fatigue experienced by the older person with MS can be significantly greater than the fatigue experienced by persons with each condition separately.

Evaluating for the presence of fatigue can be difficult as fatigue is to a large extent a subjective complaint. The use of self-report measures such as the Fatigue Severity Scale can indicate the presence of fatigue but not necessarily how it manifests itself in actual practice. Examining performance during a sustained task can alert the clinician to the impact of fatigue on that task itself. For example, a 6-minute walk test in persons with MS will often present with a slowing down of speed each minute.48 Similarly, performing balance tests such as the Berg Balance Scale in a fatigued state will result in a lower score than in an unfatigued state.49

There is no known way to accurately determine whether fatigue is primary or secondary; however, if addressing the comorbidities and secondary complications results in a relatively rapid decrease in fatigue and an improvement in endurance, that would suggest that the secondary fatigue has been addressed.

Interventions for fatigue broadly fall into 2 categories: addressing secondary complications and comorbidities, and improving overall endurance. Addressing secondary complications can include multiple areas for physical therapy evaluation and intervention. For example, clinicians should assess for the presence of tight plantarflexors and weak dorsiflexors leading to the foot drop, which can increase the energy cost of walking. Similarly, an excessively flexed posture during balance and gait will increase the energy cost of these activities and will limit the ability to perform them for prolonged periods. Other gait deviations that can increase the energy cost of walking include shortened step and stride length, widened base of support, diminished or absent arm swing and trunk rotation, and decreased hip extension at push off. Many of these deviations are adopted to compensate for a perceived lack of stability, but they often result in the compensations becoming learned, leading to a chronic cycle of compensations leading to progressively slower and more laborious gait.

Improving endurance in older persons with MS is challenging, as the presence of fatigue can limit the ability to exercise at a sufficient volume to lead to change. Intermittent walking, where periods of walking are interspersed with rest breaks, can allow the person to achieve greater volume of exercise without accruing fatigue. A walking program, in which the individual performs multiple repetitions of short, relatively unfatiguing walks interspersed with rest breaks where the individual can recover, can lead to the accumulation of a greater volume of walking than if the individual walked continuously.

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Weakness

As is the case with fatigue, weakness in older persons with MS can be due to both primary and secondary causes. In MS, damage to cortical motor areas and tracts is a common disease finding. It will present with upper motor neuron signs of spasticity, hyperreflexia, and pathologic reflexes. Weakness can also occur in MS because of disuse atrophy resulting from a sedentary lifestyle. In older adults, weakness can be a primary effect of aging occurring as a result of muscle tissue being replaced by noncontractile connective tissue, or due to disuse atrophy resulting from a sedentary lifestyle. As previously noted, fatigue is present in both cases, limiting the ability to engage in rigorous strengthening programs. The picture that emerges for the older person with MS is multifactorial weakness, with primary factors resulting from both central and peripheral causes and secondary factors resulting from comorbidities and disuse.

Strength training in this population should be initiated judiciously. Although there are no contraindications for its use, starting a strengthening program in a sedentary and disabled population risks injuries that can lead to damage of unconditioned muscles and connective tissue and result in poor motivation to comply with the program. Starting with lower weights and repetitions to avoid these complications is indicated. Monitoring for fatigue and soreness should be done at every session. Progression to higher weights is not contraindicated if the in progression is gradual. The use of intermittent strengthening programs, where a relatively smaller number of repetitions are performed with frequent rest breaks, can avoid some of the limitations that occur as a result of fatigue and allows the patient to achieve a higher total volume of strength training.

It is important to realize that strength training must be coordinated with practice of the functional task that the weakness has impacted. For example, if weakness is noted in the knee and hip extensors, then strengthening of these muscles with resistance exercises should be coupled with activities where strength in the hip and knee extensors is required, such as standing balance or sit-to-stand activities.

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Thermosensitivity

Decreased physical performance and worsening of symptoms when there is an increase in core body temperature are common findings in people with MS. They not only limit the ability of persons with MS to tolerate warmer weather but also limit their ability to engage in exercise programs as these commonly result in an increase in core temperature. It is important to note that the worsening of symptoms that results with raised core temperature does not represent a true worsening of the disease but rather a transient increase in symptoms that will resolve shortly after normal body temperature has been restored. For this reason, it is inaccurate to call these heat-induced transient worsening of symptoms as exacerbations as they do not represent disease activity; the term “pseudoexacerbations” is more accurate.

Older adults also have difficulty with temperature regulation due to deterioration of homeostatic, cardiovascular, and pulmonary functions. The diminished function of the cardiopulmonary system can be offset somewhat by prescribing fitness programs designed to address these limitations. However the impairment of homeostatic mechanisms is more problematic and requires that a stable ambient temperature is maintained.

The older persons with MS are likely to have more severe thermosensitivity as they will have a combination of impaired homeostasis for temperature extremes and aging associated comorbidities of the cardiopulmonary system. Although the use of cooling garments is well supported in the MS literature, its use with older persons with MS should be done cautiously, as the damage to homeostatic mechanisms may limit the patients' ability to perceive whether they have cooled down to near hypothermic levels.

For this reason, the cooling of smaller segments, such as the hands, wrists, neck, or head, may be preferable to larger segments such as the trunk.

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Compensation versus remediation

Both MS and aging can be considered progressive diseases, with loss of function accumulating over a lifetime. In older persons with MS, the progressive loss of function is greater than that for the individual conditions, with function lost due to both primary and secondary diseases. A significant similarity of both cases is that in both MS and aging, function can be lost because of disuse and deconditioning. This is significant as it indicates that problems with body structure/function and activity limitations can occur that are not directly tied to the disease process but are an adaptation to the disease process. This suggests that a portion of the disability that exists in these patients is learned rather than an obligatory part of the disease. It further suggests that since some of these deficits are learned, with proper training and specific practice they can be “unlearned.” For example, patients who decreases the distance they walk over the course of their disease will, over time, lose walking ability in part simply because they engage in the task of walking less. Unfortunately, as their walking volume diminishes, and their walking becomes more arduous, they will often be given a wheelchair or a scooter. Although this will address the issue of increasing the patients' diminishing mobility, it will also have the effect of decreasing their overall activity. Having the wheelchair will result in their walking less, adding to the problem of deconditioning, and resulting in weaker and stiffer lower extremity muscles as a result of their being used less. This is of course not to say that a wheelchair cannot be useful for patients who have lost ambulatory function, but rather, that prescribing a compensatory device before it is actually needed can worsen some of the effects of the disease that might be remediable to treatment. Another example of this would be the patient who develops a foot drop as a result of plantarflexion tightness and dorsiflexion weakness. A foot drop places a person with MS at significant risk for falls. In this case, many patients with MS are often given an AFO as soon as a foot drop is detected. Although an AFO can improve gait stability by facilitating a good heel initial contact, it also immobilizes the ankle. This, in turn, prevents the ankle from going through normal range of motion and limiting the need for ankle muscles to contract. The AFO therefore may actually worsen the problem that it is meant to address! Again, this is not to say that there is no place for an AFO in treating a foot drop in the older person with MS; however, given the possibility that some of the reasons that the foot drop has occurred may be due to disuse, a program of plantarflexor stretching and dorsiflexor strengthening could be instituted before utilizing a orthotic intervention.

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Keywords:

age-related changes; aging; multiple sclerosis; neurorehabilitation; Parkinson disease

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