In Parkinson’s disease, the loss of dopaminergic cells in the substantia nigra affects the basal ganglia’s ability to coordinate inhibitory and excitatory neural motor signals (Kwan & Whitehall, 2011). The net effect is an overall reduction in motor output, referred to as hypokinesia. Unfortunately, drugs used to treat PD can introduce too much dopamine, causing over-activation of the motor system and producing dyskinesias (fragmented or jerky motions, spasms, or tics). The motor symptoms associated with PD affect all aspects of daily activities, gait, postural stability, and mobility.

Tremor, Rigidity, Bradykinesia, and Dyskinesia

One of the first visible motor symptoms to emerge in PD is resting tremor of a limb that is supported and at rest. Tremor typically begins on one side of the body (frequently in one hand) with a tremor rate of 3 to 7 cycles per second. Tremors are usually less severe or even absent with voluntary movement and can increase during times of emotional stress. Tremor is considered one of the cardinal symptoms of Parkinson’s disease—some studies report it to be present in up to 80% of patients with autopsy-proven PD (Dovzhenok & Rubchinsky, 2012).

Rigidity is another common visible motor symptom associated with PD. It is a type of increased muscle tone generally defined as an increased resistance to passive movement of a joint. Rigidity tends to be more prominent in the flexor muscles of the trunk and limbs, causing a characteristic stooped posture. There are two types of rigidity: lead pipe and cogwheel. Lead pipe rigidity is defined as a constant resistance to motion throughout the entire range of movement. Cogwheel rigidity refers to resistance that stops and starts as the limb is moved through its range of motion.

Bradykinesia, another cardinal motor feature of PD, is of unknown cause and remains the subject of debate. It is defined as slowed voluntary movement, although we now know that rigidity also affects automatic movements such as arm and leg swing during gait.

One theory suggests that bradykinesia is a compensatory response, intended to slow voluntary movements and improve movement accuracy. Another hypothesis suggests that it is caused by a deficit in force production. The force production theory has been contested by studies demonstrating that people with PD are able to achieve adequate muscle contractions on neurophysiologic testing. Some researchers have suggested that bradykinesia, rather than being simply a manifestation of motor slowness (movement speed and initiation), might reflect a specific neural deficit originating in the striatum (Shiner et al., 2012).

One of the striking clinical characteristics of bradykinesia is its variability, with the same patient being able to achieve perceivably different movement speeds in different contexts. An extreme manifestation of this variability is kinesia paradoxica, in which patients are suddenly able to move at near normal speeds, that can occur in extreme, aversive contexts (Shiner et al., 2012).

Among the major complications in PD is the presence of dyskinesia. Dyskinesias consist of abnormal movements (e.g., movement of the head, neck, limbs) that are debilitating, physically tiring, and embarrassing. Several reports have shown that the rate of this problem varies, ranging from 19% to 80% in PD patients (Lokk & Delbar, 2012).

Balance, Orientation, and Postural Control

Balance is the ability to automatically and accurately maintain your center of mass over your base of support. Postural orientation is the ability to control the segments of your body in relation to one another and to gravity, taking into account the environment and whatever task is being performed. Postural control involves both balance and postural orientation.

Control of posture has both musculoskeletal components (range of motion, flexibility, muscle function, and the biomechanical relationship between body segments) and motor processes, which organize the muscles into neuromuscular synergies. Balance also involves neural components—sensory and perceptual processes—that integrate input from the somatosensory, visual, and vestibular systems, as well as higher level processes that contribute to anticipatory and adaptive aspects of postural control (Shumway-Cook & Woollacott, 2012).

Poor balance and unstable posture are commonly observed motor symptoms in those with PD. Until recently, it was thought to occur relatively late in the course of the disease. This is reflected by the Hoehn and Yahr scale, in which postural instability is represented only in the advanced stages of the disease (stages 3 to 5). However, there is significant evidence that changes in postural control occur even in the early stages of Parkinson’s and, although there is fluctuation, generally increase over time (Maetzler et al., 2012).

In early-stage Parkinson’s there may be only minimal levels of functional impairment. Walking may be slowed and stride length reduced during simple movement and gait tasks. However, altered postural control is often evident during standing tasks along with difficulty in turning. Turning difficulty becomes a sensitive indicator of a higher prevalence of freezing and falling in persons with advanced PD (Song et al., 2012).

Gait Impairment

Gait changes are a hallmark of PD, with reductions in speed, decreased step length, altered cadence, and increased gait variability. While gait abnormalities are not pronounced in the early stages, their prevalence and severity increase with disease progression. Within 3 years of diagnosis, more than 85% of people with clinically probable PD develop gait problems. The potential consequences of gait impairments in PD are significant and include increased disability, increased risk for falls, and reduced quality of life (Kelly et al., 2012).

As the disease progresses, people with PD typically exhibit shuffling gait with a forward-stooped posture and asymmetrical arm swing (festinating gait). These characteristics use a lot of energy, so that routine walking places a person at or near their maximum metabolic capacity (Hass et al., 2012). Gait impairments are compounded by the presence of bradykinesia, rigidity, and postural instability (Shumway-Cook & Woollacott, 2012).

In kinematic studies of those with Parkinson’s disease, these gait alterations are commonly observed:

• Lack of heel strike—foot lands either flat or forefoot lands first
• Incomplete knee extension during stance phase
• Inability to extend the knee and flex the ankle in terminal stance
• Forward trunk lean
• Lack of motion in the trunk
• Reduced or absent arm swing
• Decreased toe clearance
• Reduced speed and amplitude (Shumway-Cook & Woollacott, 2012)

Single-task walking deficits, in which no other task besides walking is required, have been associated with a variety of motor symptoms in PD. For example, increased rigidity is associated with poorer performance on single-task measures of balance and functional mobility. Rigidity may contribute to reduced lower-extremity joint excursions and a forward flexed posture when walking. Bradykinesia can lead to shortened step length and reduced gait speed during walking. Postural instability may contribute to gait impairments such as increased stride-to-stride variability and double limb support (Kelly et al., 2012).

Balance and gait abnormalities can lead to reduced quality of life. In fact, people with PD consider mobility and walking limitations to be among the worst aspects of the disease (Kelly et al., 2012). Patients consistently identify improvement in walking as the most relevant outcome when rating the success of a Parkinson’s treatment (Hass et al., 2012).

Freezing of Gait

Freezing of gait (FOG) is the periodic inability to generate effective stepping. It is consistently seen as one of the most disabling and distressing symptoms of PD. Patients often describe FOG as a feeling that their feet are “stuck to the floor”; or “glued to the ground” despite attempts to force themselves to walk. FOG increases with duration of disease; approximately 30% of PD patients experience FOG within 5 years, and nearly 60% after 10 years (Lo et al., 2010).

FOG is chiefly triggered at the onset of walking and during turning, but also when confronted with narrow spaces (such as doorways) or when approaching targets. Its duration is usually less than 10 seconds and rarely longer than 30 seconds. Administration of L-dopa can reduce FOG, which is more common when medications wear off, suggesting dopamine deficiency as a cause (Arias & Cudeiro, 2010).

Clinical management of FOG is limited in large part by the difficult nature of assessing its severity, and subjective measures have dominated the field. Item 14 (part III) of the Unified Parkinson’s Disease Rating Scale (freezing when walking), rates patients on a scale from 0 (none) to 4 (frequent falls from freezing) based on clinical history. This was the primary outcome measure (UPDRS 14 ≥1) used in a large study of selegiline* as a prophylactic treatment for FOG in early PD (Moore et al., 2013).

*Selegiline (a MAO inhibitor) is used to help control the symptoms of Parkinson’s disease in people who are taking levodopa and carbidopa combination (Sinemet). Its use is discussed in detail later.

A number of prediction studies have shown that postural control deficits and freezing of gait (FOG) are powerful determinants of recurrent falls. A FOG episode can present itself by a significant step size reduction (shuffling gait), knee trembling, or complete akinesia, all leading to a sudden arrest of walking. During freezing, the center of gravity may continue to move forward while the feet stop moving; this leads to imbalance that cannot be corrected by compensatory steps and therefore increases the risk of falling. In one study, patients with PD failed to initiate compensatory stepping and exhibited FOG-like trembling knee movements when balance was challenged using a sudden forward platform movement. These findings suggest a postural control deficit and, more specifically, a failure to couple balance and voluntary locomotor synergies (Vervoort et al., 2013).

Postural control deficits in those with FOG can also occur during voluntary weight shifts. As part of a repetitive stepping task, freezers show rapid, small, and inefficient weight transfers between legs that are associated with freezing episodes. In addition, both peripheral proprioceptive feedback and central sensory processing abnormalities have been attributed to postural control deficits in PD (Vervoort et al., 2013).

A Freezing of Gait Questionnaire (FOG-Q) and the new FOG-Q (NFOG-Q) have recently been proposed as sensitive tools to identify FOG behavior and assess the efficacy of interventions. However, neither the FOG-Q nor NFOG-Q score correlated with the severity (frequency or duration) of freezing episodes during actual walking in a recent study of PD patients with self-reported FOG (Moore et al., 2013).

Evaluation of video recordings of ambulating patients has been used to identify the number of FOG events utilizing one, two, or three observers. This technique has emerged as a de facto gold standard in the past decade. A recent study utilizing ten experienced raters across four leading PD centers who assessed videos from “freezers” found only moderate inter-rater agreement for number of FOG events, and intra-rater reliability was remarkably low (Moore et al., 2013).

Current treatment options for FOG are largely ineffective. Increased prevalence of freezing is observed in advanced disease and in the clinical “off” or un-medicated state, highlighting the key role of striatal dopamine depletion in its pathogenesis. Increasing levodopa dosage can reduce the frequency of off-state freezing without altering the underlying pathophysiology, likely by increasing the threshold for FOG to occur. However, FOG commonly shows only partial response to levodopa, and the benefits of increasing levodopa dosage in reducing FOG must be balanced with the increased likelihood of levodopa-induced dyskinesias, also associated with a greater fall risk (Moore et al., 2013).

Patients may undergo deep brain stimulation surgery to relieve symptoms of off-state FOG, although these surgical interventions are currently viewed as a treatment option only in the later stages of PD. Clinical management of dopaminergic therapy to minimize FOG, as well as the evaluation of new targeted interventions, would benefit from the development of objective, standardized FOG measures capable of monitoring this debilitating symptom in a community setting (Moore et al., 2013).

Difficulty with Dual-Task Walking

[This section taken largely from Kelly et al., 2012.]

Several studies have looked at gait impairment when walking is performed simultaneously with another task, referred to as dual-task walking. Dual-task walking requires the simultaneous performance of walking and another physical or cognitive task. Concurrent cognitive tasks can include mental tracking, arithmetic calculations, conversational tasks, and memory tasks. Concurrent motor tasks can include carrying objects or manipulating objects while walking.

People with PD report that walking while performing another task is one of the greatest challenges of daily mobility. They also describe the need to use concentration to monitor and correct walking, consistent with James Parkinson’s original observation that “walking becomes a task that cannot be performed without considerable attention.”

Several mechanisms specific to PD may contribute to dual-task walking deficits. One such mechanism is referred to as reduced movement automaticity. Automaticity is the ability to perform a skilled movement without conscious or executive control or attention directed toward the movement.

The basal ganglia are proposed to play a key role in the automatic control of movement. Basal ganglia dysfunction may lead to reduced movement automaticity and the need for increased reliance on cognitive resources to control movements. If reduced movement automaticity contributes to dual-task walking deficits in people with PD, rehabilitation strategies designed to improve the automatic control of walking should improve dual-task walking.

Dopamine-mediated dysfunction of the basal ganglia may also contribute to dual-task walking deficits in PD. Degeneration of dopaminergic neurons in PD appears to affect both motor and cognitive circuits within the basal ganglia. Dual-task walking deficits are improved by antiparkinson medications, supporting the idea that motor and cognitive impairments are due in part to dopaminergic pathways. The impact of antiparkinson medications may be limited to those impairments mediated by dopamine dysfunction, and many studies demonstrate dual-task walking deficits in people with PD in the “on” medication state.

The presence of non-dopaminergic pathology, which may affect both gait and cognition, may also contribute to dual-task walking deficits in PD. It is increasingly thought that the pathology of PD is not limited to dopamine but includes other neurotransmitter systems such as serotonin, norepinephrine (noradrenaline), or acetylcholine. Dysfunction in multiple neurotransmitter systems may contribute to gait and cognitive impairments. Consistent with this idea, dual-task walking deficits persist even when people with PD are optimally medicated.

Community Walking

[This section is based on Lamont et al., 2012.]

People who have Parkinson’s disease face a variety of challenges in the community. Independent functioning is related to our ability to walk efficiently, and community walking enables us to participate in a range of societal, work, and leisure activities. This includes the ability to negotiate public and private venues, both indoors and outdoors, that present a variety of environmental demands. People with PD often find environmental barriers to walking in the community but tend not to report disability; rather, they modify their behavior.

Current clinical methods of assessing community mobility that focus on gait speed or distance may not provide sufficient information to accurately reflect a person’s ability to walk in the community. A deeper understanding of preclinical walking disability may allow therapists to provide more timely assessment and therapy, delaying the onset of disability rather than attempting to reverse disability after it presents.

A recent Australian study looked at factors that contribute to a person’s ability to walk in the community. Eighteen participants with PD were asked which factors help or hinder their community mobility. Participants considered several factors associated with successful community ambulation, including walking speed, planning and preparation, traveling on holiday, medication management, the role of a partner, pedestrian crossings, and barriers to community walking.

Paying Attention to Walking Speed

A common strategy reported by study participants was the need to consciously pay attention to walking speed, step length, and toe clearance. Most people reported that they either concentrated on their walking or took extra care with walking. Consciously taking long, rhythmical steps was commonly used to aid walking in the community but several participants reported that using this strategy in a community environment was less automatic than when at home (Lamont et al., 2012):

“If you walk slower, and lift your feet and concentrate, that helps.”

“. . .you’ve got to try and think and remember to do it, like, think and make sure you do it. . . try and step it out and lift your feet more.”

Planning and Preparation

Study participants noted that planning and preparation played a key role in the success of community ambulation. Almost everyone reported planning outings to coincide with times of high medication effectiveness (“on” times). Being prepared for outings and making a plan and keeping to that plan reduced the chance of running late, feeling rushed, and making errors such as forgetting to take medications. Errands were also carefully organized to ensure the shortest walking distance. Study participants reported feeling less stress when these strategies were employed (Lamont et al., 2012).

Traveling on Holiday

Community walking related to a novel or enjoyable situation was discussed by several of the study participants and supported by their partners. Specifically, participants described reduced symptoms and less fatigue while traveling on holiday than they generally experienced at home, a change which could last for a number of weeks after their return (Lamont et al., 2012):

“Going back three years when [my wife], I’d say, had full-blown Parkinson’s, she was very, very bad. We took an overseas trip and. . . [my wife] just kept going and going. By the time we got to France I flaked. . . She still kept going. . . Something kept her going because as soon as we got home, boom, she got Parkinson’s again, but while we were away it didn’t seem to affect her.”

Optimal Medication Management

The reported effects of antiparkinson medications on walking were variable. Medications improve some aspects of single-task walking, including gait speed and stride length, but may not influence other aspects, such as stride-to-stride variability, festination, and freezing of gait. Optimal medication management was related to a more efficient gait pattern and less fatigue, making long-distance walking more feasible. A positive response to surgical intervention allowed one study participant freedom from a schedule of medication, permitting community outings to occur at times convenient for reasons other than medication effectiveness (Lamont et al., 2012):

“I love it, I love the independence and I love being able to go to the shops and not be dictated by the medication.”

The Role of a Partner

Several of the study participants and their partners reported that the partners played a crucial role in mobility by encouraging the participant to go out, promoting the importance of walking, providing physical assistance to overcome barriers in the environment, and supporting the use of attention or cueing strategies. Effective cueing strategies were discrete, mutually agreed upon, and practiced to avoid using a counterproductive cue (Lamont et al., 2012).

Pedestrian Crossings

Only one aspect of the physical environment was described as a facilitator to community walking, but this was reinforced by most of the study participants: pedestrian crossings with signals. Participants reported that signaled pedestrian crossings reduced the attention required to monitor traffic and decide when to cross safely and therefore facilitated walking in the community. For a number of participants, this had become a habit, now done without compromise (Lamont et al., 2012):

“. . .you never try to run a light, you always wait for the lights, and you don’t cross any road if there is not a light.”

Barriers to Community Walking

Participants reported a number of external barriers when walking in the community. Crowded environments were overwhelmingly disliked. Participants described that the need to change direction and avoid obstacles when walking in cluttered or heavily populated environments was a trigger for short, shuffling steps and more frequent episodes of freezing (Lamont et al., 2012):

“I find it more difficult when there are a lot of people around, it means you have to take shorter steps. I like taking long steps, I can balance myself better.”

Characteristics of the walking surface, such as uneven footpaths, hills, ramps, moving walkways, and slippery surfaces, were reported as a cause of increased fatigue, fear of falling, and more frequent freezing episodes. Even the camber of the footpath, designed to allow water to drain, was commonly reported to make walking more difficult (Lamont et al., 2012):

“My greatest difficulty when I’m walking is going downhill. Can’t handle it. I can go uphill flat out, but I can’t handle going downhill. Even with a trolley my feet get stuck on top of a ramp and I can’t get going.”