Locomotor training in people with Parkinson disease.

The purpose of this article is to consider the role of the physical therapist in locomotor training for people with idiopathic Parkinson disease (PD), taking into account how therapy can be adapted according to disease progression, medication status, environmental conditions, and the goals of the locomotor tasks being performed. Using the World Health Organization's International Classification of Functioning, Disability and Health (ICF), (1) locomotor training will be considered in relation to impairments of body structure and function, activity limitations, and participation restrictions. Analysis will span the de novo stage, early in the disease process before levodopa or other PD medications have commenced, through to end-stage disease, which is often 20 to 30 years later.

Locomotor disturbance is an early sign of PD, (2,3) yet it can easily be overlooked in elderly people. Due to a progressive loss of substantia nigra neurons that produce dopamine, neurotransmitter imbalances occur in the basal ganglia. (4) Once around 80% of neurons have been lost, PD becomes evident and people begin to experience difficulties with motor skills, cognition, and autonomic function. (5) Sensory, emotional, and perceptual signs also are observed in some individuals. (6) Footsteps become asymmetrical and underscaled in size and speed (hypokinesia), difficult to activate (akinesia), and difficult to terminate and show progressive diminution as the locomotor sequence progresses. (6-9) Resting tremor, rigidity, and, later in the disease process, postural instability and falls also are characteristic of PD. (10,11)

As illustrated by the Figure, these impairments of body structure and body function are associated with limitations in activities such as walking in the home and community, moving from a lying to sitting to standing position, and turning. (12) Functional activities that require the performance of motor skills become compromised even though the ability to perform simple movements is retained. This is because simple movements are controlled by frontal, cerebellar, and brain-stem regions rather than the basal ganglia, (13) and these regions are not affected in the early stages of PD.

[FIGURE OMITTED]

Secondary to aging, immobility, and disuse, locomotion also can be affected by musculoskeletal impairments such as weakness, reduced flexibility of joints, and deformity as well as cardiopulmonary impairments such as reduced aerobic capacity. (14,15) In turn, these impairments and activity limitations restrict the person's ability to participate in societal roles related to work, family life, education, civic life, and leisure. (16) Although levodopa and other PD medications are initially very effective in reducing the severity of movement disorders, some gait disorders persist despite optimal medication. (17,18) The Figure summarizes these interactions and shows how performance within these domains of the ICF is influenced by individual factors such as the person's age, disease duration, PD medication, and socioeconomic status in addition to environmental factors such as their level of supervision and the physical environment in which locomotor tasks are performed.

Several systematic reviews and conceptual articles have shown that physical therapy aims to teach people with PD how to minimize the disabling effects of motor and sensory impairments in order to enhance participation in societal roles and quality of life. (3,16,19-22) This is based on emerging evidence in animal models that pharmacotherapies, learning, and exercise may have a neuroprotective influence in neurological disorders. (23-25) For example, Woodlee and Schallert (23) found the onset of abnormal movements to be prevented or delayed when parkinsonian rats exposed to MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) were trained in an enriched environment. Similarly, rat models of Huntington disease have shown that locomotor training using a treadmill within an enriched environment delays the progression of gait disorders. (25) It has been argued that early treatment targeting up-regulation of dopamine neurons might slow down the progression of the PD. (23) Research on neural adaptation thus raises the possibility that goal-directed, learning-based training can contribute to enhanced function in people with neurodegenerative conditions. (24)

Locomotion in Parkinson Disease

Even before the diagnosis of PD has been confirmed by a neurologist, most people with the disease find that they are walking more slowly than usual and with short steps. Their shoes frequently scuff the ground, and they are susceptible to tripping on obstacles. (26) The trunk is held rigidly, the width of the base of support narrows, and there is a high stepping rate. (27) In addition, people with PD can experience difficulty initiating and terminating a step (akinesia). (28) As the disease progresses, there is asymmetry and reduced amplitude of arm swing. (29) Overall, gait patterns become increasingly stereotyped, and there is reduced flexibility in adapting to new environments or task conditions.

These gait disorders are most pronounced for well-learned locomotor sequences, such as walking and turning (12) or walking while performing a secondary task such as talking, (30) carrying a tray, (31) or transferring coins from one pocket to another. (32) Reduced gait speed and shortened step length tend to be more accentuated in the "off phase" of the levodopa cycle, when the neurotransmitter imbalance in the basal ganglia is most pronounced. (33-35) Other gait variables, such as footstep timing, are less affected by PD and are less responsive to PD medication. (36)

Gait disorders also vary according to the environment in which movement occurs. (29) Although people with PD can walk relatively quickly and easily in open spaces or very familiar environments, the slow-stepped shuffling gait pattern that is so characteristic of the disease re-emerges in novel environments or congested spaces. (29) This is because the role of the caudate in processing multiple sensory stimuli and motor skill learning is disrupted. (37,38) Unexpected changes in the ground surface, walking slope, pathway width, or lighting conditions can be problematic, particularly in elderly people with advanced disease who have postural instability. Changing the goals or complexity of the locomotor task can be challenging when there is insufficient time to use intact frontal cortex regions to plan adaptations to the stepping pattern. The defective basal ganglia also compromise the person's ability to quickly shift from one mode of locomotor behavior to another. (39-41) For this reason, people with PD can experience difficulties in changing from walking slowly to walking quickly, making the transition from hard to soft floor surfaces, or veering to avoid an obstacle.

Physical Therapy for Patients With Newly Diagnosed Parkinson Disease

In the early months after diagnosis, physical therapists have considerable scope to teach people with PD strategies to optimize locomotor performance and physical activity prior to the commencement of levodopa medication. Uniquely, in the "de novo" stage, there is an opportunity to assess the person's baseline levels of impairments, activity limitations, and participation restrictions before medications have commenced. The natural variability in the person's capabilities, therefore, can be mapped without the confounding effects of pharmacological therapies. Baseline data can be retained for future use in evaluating disease progression. (42) Core strategies can be learned for moving quickly and easily with large-amplitude movements, (19,43) and these strategies can be retained for when they are needed later in the disease process.

At the time of diagnosis, disease progression is usually minimal, which arguably provides physical therapists with the best opportunity to take advantage of the capacity for motor skill learning. In the early stages of skill acquisition, frontal cortical regions are used to control movements using attentional processes. (13,44) With practice, control is relegated to the basal ganglia, allowing movements to be executed quickly, easily, and automatically. (37,44,45) When the basal ganglia are dysfunctional, as in PD, automaticity of movement is compromised and there is greater reliance on frontal-lobe attentional mechanisms to control movements. Thus, people with advanced PD have difficulty learning a skill, task, or strategy to the stage that it is retained over long periods and generalized to the performance of similar tasks. (46,47)

The motor learning literature shows that skills are learned most effectively when they are practiced repeatedly in relation to meaningful goals, incorporating variations in the manner in which they are performed and varying the environment and task. (37,46,47) For example, if the goal is to train a person with gait hypokinesia to walk with long steps, this could be practiced repeatedly over short (eg, 10 m) and longer (eg, 40 m) distances on different walking surfaces (concrete, floor boards, carpet, grass, uneven ground, slopes) at slow, medium, and fast speeds. The person with mild PD also could be encouraged to walk with long strides on wide and narrow pathways, incorporating turns of different magnitude (eg, 60[degrees], 120[degrees], 180[degrees]) rather than simply performing straight-line walks. (48)

If a person has gait hypokinesia, visual cues also can be used to enable him or her to walk with long steps. (29) Evidence has accumulated showing that visual cues can normalize step length for several minutes to several hours. (17,30,49,50) Moreover, a single-case study by Sidaway et al (51) showed that 4 weeks of daily gait training led to long-term improvements in step length and speed. Visual cues in the form of white strips can be very effective when taped to the floor (eg, in the corridor that leads from the bedroom to the toilet) or other areas where people fesfinate or have poor gait initiation. Some people find it useful to place small signs on the wall close to a door where troublesome freezing episodes occur to remind them to "take long steps." (52) Van Wegen et al (17) reported that rhythmically flashing lights as well as projection of virtual stripes on the floor could be used to enhance step length in people with PD. Of interest, in the early stages of the disease, people find ascending and descending steps relatively easy because the stairs act as visual cues that drive motor performance. (53)

The attentional load is considered to be a key constraint to motor performance in PD. (45,54-56) For people with mild PD, it could be useful to encourage concurrent activities with the aim of enabling them to learn multitasking. Practicing walking with attention directed toward secondary tasks of increasing levels of complexity also could be built into the training regimen, provided that the person has sufficient cognitive ability to be able to learn how to safely perform more than one task at a time. (19) Examples include training people to maintain long strides while performing a secondary task such as talking on a cell phone, carrying a tray, or transferring coins from one pocket to another. (45) This type of intense, variable, and distributed practice regimen appears to provide the best conditions for acquiring and retaining flexibility and adaptability in locomotor control. (55,57) As will be discussed, when the disease has become advanced, it is safer to teach people with PD to avoid dual task intervention by focusing on performing only one movement at a time.

Instructional sets (58,59) are another powerful determinant of performance in PD, and some walking trials can be performed while the physical therapist says "long strides," (30) "think big," (35) or "step out" and other walking trials could be performed with the person using his or her own internally generated instructions or mental images of long steps. (29) In addition to practicing walking in the physical therapy clinic, the person could be encouraged to walk with long strides around the home and in the community. (35) Practice of both treadmill and overground walking also can be considered for people with mild PD, with or without a musical beat to motivate performance. There is preliminary evidence that treadmill training enhances stride length and gait speed in people without balance impairment, (60-63) although this awaits replication.

From the outset, it is recommended that information be provided about falls prevention, the future risk factors for falls, and how to modify the environment and task performance in order to avoid slipping, tripping, and falling. (19) Activities such as walking, cycling, golf, tai chi, and bowling also can be practiced. (19) Another priority is to educate people with PD and their "significant others" about the benefits of regular physical activity and how to incorporate into their life a daily exercise and mobility routine. (59) Progressive resistance strength training has been shown to have beneficial effects (64) even though weakness is secondary to disuse rather than a primary outcome of PD.

Physical Therapy After Levodopa Is Commenced

On commencement of levodopa or other PD medications, the physical therapist acquires several new roles. The first new role is to evaluate the person's response to the medication by conducting a dose-response trial. (65) We have provided details on how this involves measuring impairments of body function and activity limitations at close and regular intervals across a 24-hour period when the person is both "off" and "on" his or her medication. (65) For example, the neurologist might refer the person for evaluation of changes in walking speed, step length, tremor, dyskinesia, and balance at 15-minute intervals early in the morning after a 12-hour period in which medication has been withheld and then throughout the same day after the medication has been administered. By graphing or tabulating the person's response to medication for these variables, the physical therapist is able to provide medical practitioners and other health care professionals and the person with data about the positive or negative effects of medication. This can enable the type and dosage of medication to be carefully adjusted to the person's needs while avoiding undesirable movement disorders such as dyskinesia, dystonia, or hypokinesia. It also provides physical therapists with information about the residual movement disorders that are still apparent despite the best possible medication regimen. In turn, this can aid clinical decision making and assist the physical therapist and patient in determining the priorities and goals of treatment together.

Another role is to educate the person about the presence and timing of symptoms and possible ways to overcome them. (19) Attentional strategies such as focusing attention on the key aspects of the gait pattern requiring improvement, avoiding the performance of a secondary motor or cognitive task that may compromise safety during gait, and breaking down long or complex locomotor sequences into component parts and concentrating on the performance of each part can enable people to walk more easily. (19,56) Visual cues continue to be helpful as gait hypokinesia and akinesia progress in severity. (29)

At this stage, gait freezing emerges as a problem in some individuals. Auditory cues that aim to normalize locomotor timing such as provided by a musical beat or rhythmical chanting can help some people move more easily. (66-70) Nieuwboer et al (68) found that premature timing of the tibialis anterior and gastrocnemius muscles occurs just before a gait freezing episode due to a disturbance of central locomotor timing mechanisms and that auditory cues provide one mechanism for overcoming this. Moreover, Fernandez del Olmo et al (71) reported reduced movement variability in 9 people with PD after a 4 week program of daily gait training using auditory cues, and this finding correlated with changes in regional cerebral glucose utilization as shown by positron emission tomography scans.

With disease progression, some patients exhibit difficulties with gait termination. They show excessive diminution of the footstep size and speed prior to a planned stop and overshooting of step length at the termination point. For example, when approaching a chair with the intention of turning around to sit down, the person's footsteps are dramatically reduced in size and speed and freezing occurs prior to and during the turning maneuver. The person might benefit by planning and mentally rehearsing the procedure for terminating the straight-line walking sequence and performing the turning and sitting down components separately. (19) Freezing just short of a goal, such as sitting down, also can be avoided by focusing on the far arm of the chair when walking toward it.

Physical Therapy 5 to 8 Years After Medication Commences

Although levodopa and other PD medications are usually very effective initially, motor fluctuations eventually occur because the progressive death of substantia nigra cells continues despite optimal pharmacological interventions. Performance varies throughout the day and from one day to the next, (27,72) and the performance of complex motor tasks can become intermittently problematic. Physical therapy at this stage aims to teach people how to increase movement speed and amplitude, optimize postural alignment, and maintain postural stability at the times when the medication is not holding them within the normal range. Therapists also can train people with PD and their significant others to identify when movements, postural alignment, or balance are within a pathological range, as self-monitoring of motor performance is not always optimal. This is particularly relevant for people who are frequent fallers, who can benefit from being trained to deliberately monitor their walking patterns and balance during tasks such as turning to avoid tripping and falling.

Around 29% of community-dwelling older adults who are healthy fall each year, (73) compared with up to 60% of community-dwelling people with PD. (18,74,75) One study (76) showed that a quarter of people with PD experience fractures in the first 10 years after diagnosis. Most falls in the PD population occur during the day and indoors, when people are most active and at their best clinical condition at peak dose. (77) Fewer falls occur at the end of dose or during the "off" phase of the levodopa cycle, when patients are less mobile. Although gait parameters such as step length are responsive to levodopa, postural instability shows little change with medication. (78,79) Environmental factors predict falls to a moderate extent in people with PD, whereas rapid turns, complex tasks, and transfers appear to be more highly correlated with falls. (77) To minimize the rate and severity of falls, home environments can be cleared of excessive furniture and trip hazards. (19) Changes in support surfaces (such as carpet to floorboards) can be highlighted by using brightly colored tape to direct the person's attention toward his or her footsteps, as changes in environmental context such as this (or a narrow doorway) appear to trigger freezing episodes that increase the risk of falls in people with akinesia. (80) When approaching doorways, short shuffling steps can re-emerge, and it can be useful to encourage people with this form of motor instability to look past the doorway at an object in order to avoid hypokinesia and freezing. In addition, footwear can be checked to ensure that it is supportive and not too tight or loose.

Given the marked variability in performance that typically occurs after 5 to 8 years of PD medication, (29,81,82) there is a need to devise and evaluate locomotor training programs for both the "on" and "off" phases of the levodopa cycle. Even when patients are fully medicated and in the peak dose of the medication cycle, they still have gait disorders (27,34,83) and dual-task interference (45) that warrant treatment. This is the major reason why physical therapists and other allied health professionals provide gait training as an adjunct to pharmacological therapy in everyday clinical practice. Because most people with PD show differences in their performance when they are "on" compared with when they are "off" the medication cycle, it can be useful for the physical therapist to color code their assessment and treatment planning documentation and to teach them separate strategies for when they are "on" or "off" the medication cycle. (19,29)

At the end of the dose, many patients experience gait hypokinesia (slowness with reduced amplitude), gait initiation and termination difficulties, and freezing. Some patients have dystonia of the plantar flexors, reduced arm swing, or rigidity of the trunk. (84-86) At peak dose, some people have no residual movement disorders, whereas others experience slowness and other impairments despite the best possible pharmacological regimen. It is very important to document the time of physical therapy measurements together with the times for PD medications on that day so that judgments can be made about whether a person's performance is better or worse for that point within the medication cycle. (19,29) Given the variability in performance in people with PD, it is necessary to know when assessments are made in order to judge whether they are responding favorably to treatment.

Turning during locomotion is typically problematic in the early and middle stages of disease progression and can be associated with trips, falls, and freezing episodes. (12,29) Turning disorders and falls are presumably not as common in the advanced stages of disease progression because patients are not so mobile then. (87) Using 3-dimensional motion analysis, Huxham (87) measured self-paced 60-degree turns during walking in people with PD compared with young and older adults without impairments. Those with PD showed shorter step lengths and reduced axial rotation at the pelvis as well as diminished counter-balancing activity at the thorax, even for this relatively small turning angle. Strategies to improve performance during gait include deliberately turning in a large arc of movement rather than rapidly swiveling on the spot, planning the turn so that it is performed using planned control mechanisms rather than attempting to turn automatically "on line," and using visual cues (such as looking at a chair or obstacle on the ground) to assist the direction change. (19,57) In addition to avoiding the performance of secondary tasks, the person can be encouraged to turn gradually rather than sharply. This appears to be the preferred strategy for all age groups when the turn path is not predefined.

Advanced Disease Progression

Because the loss of dopamine-producing neurons in the substantia nigra progresses over time, gait disorders become more severe and variable in their presentation in the advanced stages of the disease. (33) Severe gait hypokinesia is very common, and most people find that their footsteps are shortened and the ground clearance is diminished toward the end of dose or in the half hour after it has been taken, before a sufficient level of uptake has occurred. (19) The strategies for hypokinesia described earlier are applicable, although particular attention needs to be directed toward preventing trips during walking. Emphasizing dorsiflexion at heel-strike and strengthening the dorsiflexors using progressive resistance strength training may be productive. Other strategies include teaching the person how to deliberately increase the ground clearance by increasing the length of steps, planning the walking task, and carefully scanning the environment for hazards prior to and during walking. (19,29) The person can be educated about the ways in which multitask performance increases the risk of slips, trips, and falls, as well as the need to be particularly vigilant at the end of dose.

After many years of anti-PD medication, some people experience extra movements such gait dyskinesia, whereby excessive large-amplitude choreiform movements occur. (29,88) On clinical examination, the steps appear to be very long, the base of support is wider than usual, the arm swing amplitude is increased, and the magnitude of trunk rotation is increased. Many people find these large-amplitude writhing movements disconcerting from a cosmetic point of view and believe that they increase fatigue and lassitude. (89) For this reason, severe dyskinesia can be a key factor that restricts participation in social activities and community life. Unfortunately, little is known about the pathogenesis of gait dyskinesia or its response to physical therapy. There is a clinical impression that relaxation techniques are helpful for providing short-term relief from dyskinesia, (99,89) although this has not yet been confirmed with controlled clinical trials. Focusing attention on keeping still, weight bearing, and compression reduce the size and frequency of extra movements, although the effects appear to be transient, lasting for less than 30 minutes. (19,29) Similarly, severe tremor appears to respond for brief periods to attentional strategies such thinking about keeping the limb still, mental imagery, and relaxation. (89,90) Dystonia also occurs in select muscle groups in some people with advanced disease. Prolonged stretch is reported to be useful for some people with dystonia, (89) and sensory stimulation provided by a firmly fitting sock has been noted to be useful for short-term alleviation of dystonia, (89)

Assistive devices, such as wheeled walking frames, are an option for people who are at high risk for falls. (91) They should be considered only after other physical therapy strategies for enhancing gait and balance have been attempted. Walking sticks (whether single-point or 4-point) usually provide little assistance for people with postural instability because they typically end up being carried by the person and can become a distracting source of dual-task interference. (92) Walking frames that do not have wheels also can be difficult for people with PD to use because they require the person to pick up the frame, place it strategically, and then step forward in a sequential action that is difficult for people with basal ganglia dysfunction. Likewise, forearm crutches offer little help because they require the person to repeatedly perform a long action sequence. Sometimes walking frames with front wheels can be an effective tool for enabling the person to maintain balance while walking relatively easily. (89) This appears to be particularly the case for people with cognitive impairment who cannot learn other strategies to maintain balance and safety.

In some people with advanced disease who are troubled by disabling dyskinesia, tremor, or dystonia, brain surgery can be an option. Due to the usual risks associated with neurosurgery, most candidates are younger people with rapidly progressive PD or older adults who need surgery in order to maintain employment or other societal roles. Pallidotomies and subthalamic stimulation are commonly used, (93) with varying outcomes. Reconstructive neurosurgery, such as inserting dopamine-producing neurons from porcine, fetal, or human tissue has been reported in the PD literature, although equivocal results have been obtained to date. (93) This procedure is still considered to be experimental. Physical therapists play a role in assessing motor performance before and after brain surgery "on" and "off" levodopa and other medications. In addition, the physical therapist can provide data on the amount of change that occurs in impairments, activity limitations, and participation restrictions as a result of brain surgery.

Laboratory-based 3-dimensional gait analysis (3-DGA) is used to assist clinical decision making in a small proportion of people with PD, particularly those referred for neurosurgery. Although observational gait analysis provides data on the footstep patterns and gait kinematics (angular displacements of joints and motion of body segments over time), 3-DGA provides information on movement kinetics such as the underlying moments of force and power generation in different muscle groups that contribute to the disordered movement patterns. In gait laboratories throughout the world, specialized physical therapists now play a key role in measuring locomotor performance using 3-DGA in order to quantify the outcomes of therapy, surgery, and other interventions. (94)

End-Stage Disease Management

A proportion of individuals with PD live well into very old age, and it is not unusual for a person diagnosed with PD at the age of 60 years to be coping with the interactions between long-term disease progression and aging when he or she is 85 or 90 years of age. By this time, the person has usually received physical therapy services interspersed over many years and is aware of which strategies remain helpful. Therapy now focuses on educating and supporting the primary caregiver and optimizing the person's quality of life and participation in societal roles. (19) Priorities include enabling participation in parenting and grandparenting roles as well as assisting them to maintain relationships with their spouse, friends, and community-based organizations. There is less emphasis on the treatment of impairments of body structure and body function, unless these impairments are causing particular problems such as pain, difficulty swallowing, or difficulty breathing. Strategies for minimizing activity limitations usually involve training nurses or family members how to help the person move from one position to another and to perform daily activities such as dressing, eating, and grooming. Toward the end of life, some people with PD lose the capacity to walk safely and benefit from being prescribed a wheelchair that enables them to continue to participate in family and community activities. As with the previous stages, the physical therapist works in partnership with people with PD, their families, and other members of the interprofessional team to set therapy goals that best meet their needs without raising hopes for unrealistic levels of movement recovery. (95)

Clinical Research

Finally, it is recommended that physical therapists become more involved with clinical research, translational research, or collaborative basic science studies relevant to evidence-based practice in PD. This article has shown a paucity of physical therapy outcome studies, and there is an immediate need for controlled trials to determine optimal methods to reduce falls and enhance mobility in this debilitating disease.

Conclusion

This perspective article has integrated clinical research findings to provide clinicians with a practical guide to physical therapist management of locomotor disorders in people with PD. Although there is evidence in animal studies that aggressive learning-based activities can be neuroprotective, to date there are no longitudinal clinical studies confirming that a meticulous commitment to learning in a patient diagnosed with PD would actually slow down the progression of the disease. There are many characteristic features of PD gait, and large individual differences exist in the combinations of gait deviations seen and the extent to which locomotor performance fluctuates over time.

Physical therapists assess people with PD individually, taking into account their medication status, their changing levels of performance, their goals, and the needs of their "significant others." Goals are set and constantly modified in conjunction with the person, and therapy is regularly adjusted to minimize impairments and to increase the ability to perform functional activities. Part of the training program involves structuring the environment and controlling the ways in which tasks are performed to enhance performance. The ultimate goal is to optimize quality of life and participation in social roles pertaining to family life, leisure, work, education, and community service at appropriate stages in the life cycle. Physical therapists should collaborate with basic science researchers to improve our understanding of how movement strategies and exercise can be maximally protective and rehabilitative along with new technological and pharmaceutical interventions.

This article was received August 30, 2005, and was accepted June 5, 2006.

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M.E. Morris, PT, PhD, FACP, is Professor of Physiotherapy, The University of Melbourne, 3010, Melbourne, Victoria, Australia, and Director of Allied Health Research, Rehabilitation & Aged Care Program, Southern Health, Kingston Centre, Warrigal Rd, Cheltenham, 3192, Australia.

Address all correspondence to Dr Morris at: [e-mail].

The author acknowledges Frances Huxham, Fiona Dobson, Jennifer McGinley, Margaret Bruce, Robyn Gardiner, Pamela Fok, Pagamas Piriyaprasarth, and Dharani Kandasamy for their valuable feedback when preparing the manuscript.

This article is based on a presentation at the III STEP Symposium on Translating Evidence Into Practice: Linking Movement Science and Intervention; July 15-21, 2005; Salt Lake City, Utah.