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Rehabilitation Interventions in Parkinson

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Focused Review

Rehabilitation Interventions in Parkinson Disease

Alex Moroz, MD, Steven R. Edgley, MD, Henry L. Lew, MD, PhD, John Chae, MD,
Lisa A. Lombard, MD, Cara Camiolo Reddy, MD, Keith M. Robinson, MD
Objective: This self-directed learning module provides an evidence-based update of
exercise-based rehabilitation interventions to treat Parkinson disease (PD). It is part of the
study guide on stroke and neurodegenerative disorders in the Self-Directed Physiatric
Education Program for practitioners and trainees in physical medicine and rehabilitation.
This focused review emphasizes treatment of locomotion deficits, upper limb motor control
deficits, and hypokinetic dysarthria. New dopaminergic agents and deep brain stimulation
are facilitating longer periods of functional stability for patients with PD. Adjunctive
exercise-based treatments can therefore be applied over longer periods of time to optimize
function before inevitable decline from this neurodegenerative disease. As function deteriorates in patients with PD, the role of caregivers becomes more critical, thus training
caregivers is of paramount importance to help maintain a safe environment and limit
caregiver anxiety and depression. The overall goal of this article is to enhance the learners
existing practice techniques used to treat PD through exercise-based intervention methods.

INTRODUCTION
Parkinson disease (PD) is a common aging-related neurodegenerative disease. Its cause is
unknown; the pathophysiology has been explained by nigrostriatal pathway degeneration
associated with excessive accumulation of alpha-synuclein in specific areas of the brain [1].
The vulnerable areas include the locus ceruleus, hypothalamus, cranial nerve motor nuclei
and autonomic nervous system [1]. The mainstay of treatment is dopaminergic replacement
or enhancement. Despite the new agents that are continually being developed to augment
dopamine availability in neural tissue, as many as 50% of individuals with PD become
refractory to medical management beyond 5 years after initiation of treatment [2]. This
refraction manifests as the patient experiencing rapid motor fluctuations and/or dyskinesias
when on medication. Over the last 10 years, physiologic ablative procedures to effect deep
brain stimulation of specific nuclei of the basal ganglia (subthalamic, globus pallidus
internus) have become viewed as efficacious for up to 75% of appropriately selected
individuals who are considered medically refractory. The procedures are considered palliative, and their efficacy has been defined by stabilized function and improved quality of life
up to 5 years after surgery. For some individuals, this stabilization allows time to incorporate
exercise-based interventions as an adjunct to medical and surgical treatments. These
interventions can support functional stability before inevitable decline [3,4].
Several essential reviews of exercised-based interventions for persons with PD reported
favorable outcomes [5-8]. However, the literature is still evolving in that: (1) less than half
of the reviewed studies were randomized controlled trials; (2) about one-third of the
reviewed studies had sample sizes of fewer than 16 subjects; (3) more than half of the
reviewed studies discontinued their observations at the completion of the intervention
phases, not observing whether the positive effects of various interventions were sustained
over time. This present review provides an update of specific rehabilitation interventions in
PD supported by the literature.

MULTIDISCIPLINARY REHABILITATION INTERVENTIONS

Sunvisson et al [9] reported their observations of treatment that combined nursing education and physical therapy (PT). In a case series of 43 subjects with PD, this program
PM&R

S42

1934-1482/09/$36.00
Printed in U.S.A.

A.M. NYU School of Medicine, Rusk Institute

of Rehabilitation Medicine, New York, NY.
Address correspondence to: A.M.; e-mail:
moroza@gmail.com
Disclosure: 2, IPRO
S.R.E. University of Utah, Salt Lake City, UT
Disclosure: 2, Northstar Neuroscience
H.L.L. Harvard Medical School, VA Boston
Healthcare System, Physical Medicine and
Rehabilitation Service, Boston, MA
Disclosure: nothing to disclose
J.C. Case Western Reserve University, Department of Physical Medicine and Rehabilitation, MetroHealth Medical Center, Cleveland,
OH
Disclosure: nothing to disclose
L.A.L. Santa Clara Valley Medical Center, San
Jose, CA
Disclosure: nothing to disclose
C.C.R. Department of Physical Medicine and
Rehabilitation, University of Pittsburgh Medical
Center, Pittsburgh, PA
Disclosure: nothing to disclose
K.M.R. Department of Physical and Rehabilitation, University of Pennsylvania Hospital,
Philadelphia, PA
Disclosure: nothing to disclose
Disclosure Key can be found on the Table of
Contents and at www.pmrjournal.org

2009 by the American Academy of Physical Medicine and Rehabilitation

Suppl. 1, S42-S48, March 2009
DOI: 10.1016/j.pmrj.2009.01.018

PM&R

which consisted of twice weekly 2-hour sessions over 5

weeks resulted in significant improvements in reported
self-care, and in observed speed and integration of motor
control. These results were seen at the end of the intervention
phase and 3 months later. Moreover, significant improvements in quality of life (QOL) were observed 3 months after
the end of the intervention phase. The QOL improvements
were explained primarily by improved regulation of sleepwake cycles. Trend et al [10] conducted an open trial of
rehabilitation interventions of 118 PD patient-caregiver
pairs. The interventions, conducted once weekly over 6
weeks, encompassed a structured therapeutic day of 1-on-1
and group sessions of PT, occupational therapies (OT) and
speech therapies (ST). The sessions were conducted as a day
hospital program. Significant gains in gait, voice articulation,
and quality of life occurred during the first 6 weeks. However, when the same interventions were later subjected to a
crossover design after randomization of another 71 patientcaregiver pairs, a different outcome was observed. The same
positive effects were not observed at the 6- month cross-over
point. At 6 months postintervention gait improvements approached significance, but QOL deteriorated [11]. Moreover,
there was an increase in caregiver strain that approached
significance at this 6-month point. The difference in outcome
between the 2 studies may be due to the mistiming of the
intervention [12] or difference in rigor. Nieuwboer et al [13]
provided 2 guidelines to avoid mistimed application of
treatments. They found that (1) a higher disease severity is
negatively predictive of therapeutic benefits even in the context of a familiar home environment and (2) compromised
cognitive ability and older age were negatively predictive of
ability to sustain the therapeutic benefits of treatment. These
guides lead us to 2 conclusions. First, for older persons with
PD who are more cognitively impaired because their PD is of
higher severity, it is rational to focus rehabilitation efforts on
caregiver training. Second, for persons in middle and later
stage PD, it would appear rational to view the patient-caregiver pair as the patient.

TREATMENT OF LOCOMOTION DEFICITS

While critical reviews of PT interventions have been optimistic, many studies were methodologically flawed because of
their small sample sizes, lack of randomization, and nonuniformity of interventions, reflecting a lack of recognized standards of best practice [14-16].

External Sensory Cueing

The best studied exercise-based interventions to treat the gait
difficulties of PD are those that have used external sensory
cueing strategies, including visual (spatial) and auditory
(temporal) strategies [17]. Researchers doing gait analyses
studies have found that persons with PD experience less
central delivery of proprioceptive feedback and that 1 of the
strategies they use to compensate for that is an increased
dependence on alternative visual and auditory cues. Visual

Vol. 1, Iss. 3, Supplement 1, 2009

S43

cues are hypothesized to be a way for the person with PD to

use available neural networks that are mediated through the
cerebellum as a therapeutic bypass strategy. Auditory cues,
on the other hand, are hypothesized to be a therapeutic
restorative strategy to replace externally the degenerated
basal ganglias internal timekeeping function [18,19]. A
series of studies [20-28] on the use of compensatory sensory
systems to enhance mobility was explored in laboratory and
clinical studies on gait. These studies compared outcomes
during non-cued and cued conditions, often comparing the
performances of subjects with PD and control subjects. The
applied visual cues included floor stripes, timing lights and
mirrors; the auditory cues included music and metronomes.
Gait velocity and walking speed consistently, but not universally, improved during the cued conditions in those with PD.
Visual cues more frequently led to increased stride length,
while auditory cues were more frequently observed to increase cadence [20-28]. Visual cues were more effective at
improving gait initiation than were auditory cues [29]. However, the only studies reporting that these positive effects of
sensory cues on gait can be sustained over longer periods of
time were case studies [30].
Dual task studies in which subjects performed cognitive
or motor tasks while walking have been done [31]. In these
dual paradigm studies the researchers intent was to divide the subjects attention between the tasks and the walking action. In these studies subjects performed concurrent
tasks under cued gait training conditions. The findings from
these studies indicate that external sensory cues fundamentally enhance attention to the alternative cue during ambulation. However, the hypothesis that giving ones attention to
external, rhythmic, auditory and visual cues will somehow
either bypass or restore sensory control of movement is not
supported [31]. Other investigators critiques of these sensory cueing studies reinforce that the fundamental deficit of
gait problems in PD is attentional, and that any strategy that
enhances attention during walking will have an effect similar
to that of sensory cues [32].
Other approaches that use alternative sensory stimulation
to influence motor control are less demanding of attentional
resources. One randomized controlled crossover trial of
whole-body-vibration in 68 subjects with PD demonstrated
significant decline in clinical parkinsonian motor signs, particularly tremor and rigidity [33].

Traditional Physical Therapies (PTs)

Several clinical trials have applied a variety of exercise interventions, comparing treatment and no-treatment groups, in
subjects with PD and control subjects. Intervention phases of
treatment in these PT studies ranged from 1 to 20 weeks.
When postintervention outcomes were observed, they were
usually limited to less than 6 months after the end of the
intervention phases. Outcome measurements included gait
parameters, functional status and quality of life, and were
generally reported as improved at the end of the intervention
phases of treatment, but not consistently sustained thereafter

S44

Moroz et al

[34-38]. Several of the trials that applied novel treatments

such as partial body weight-supported treadmill training
[39,40], polestriding (walking with modified ski poles with
a movement pattern similar to cross-country skiing) [41] and
structured treadmill training [42] found these strategies to be
superior to usual PT approaches for increasing gait velocity
and improving functional status. Dibble et al [43,44] studied
the effects of strengthening in 19 PD patients randomized to
eccentric and concentric isometric strengthening groups,
who were given PT 3 days weekly over 12 weeks. In this
study eccentric strengthening was associated with greater
muscular hypertrophy and better force generation and mobility than concentric strengthening; when high-force eccentric strengthening was continued for 12 more weeks in a
subset of 10 subjects during an open trial, no clinical or
laboratory evidence of muscle damage was observed. Tamir
et al [45] compared PT-guided motor imagery in combination with exercise, and exercise alone, in a small-sample,
randomized controlled trial. The combination treatment was
more effective for reducing parkinsonian motor signs, particularly bradykinesia.

Treatment of Freezing of Gait

Freezing of gait is reported to occur in up to 50% of individuals who have PD. It is associated with higher disease severity
and longer disease progression [46]. Freezing of gait continues to be pathophysiologically elusive; however, it is well
described clinically to occur when the sensory/perceptual
demands of the environment require that a new motor program be used in order to continue a rational sequence of
movement [47]. Demands that cause individuals to freeze
include gait initiation, turning, walking through doorways,
or approaching a terminal object. Freezing of gait can be
minimized by using assistive devices, such as wheeled walkers, in combination with sensory-motor tricks. The devices
provide consistent proprioceptive delivery and the tricks
are actually behavioral strategies that can be taught to both
patient and caregivers. One such strategy helps overcome the
feeling that ones feet are glued to the ground. The person
with PD is taught not to actively disconnect his/her glued
feet from the ground, but rather to allow the motor block to
occur, momentarily relax, then re-initiate gait. During training, the person with PD is taught to use a hip/knee hyperflexion maneuver to step out and over an imagined or real visual
cue. The cue may be, for example, a self-triggered laser beam
at ankle level generated from the wheeled walker or cane or a
low physical barrier, such as a yardstick laid flat on the floor
[48,49]. Empirically, the presence of the sensory cue does
not appear to be as essential as using the proximal leg flexors
to re-initiate gait.

Treatment of Deficits in Postural Control

and Balance
Several open clinical trials have focused on observing postural control and balance during and after exercise inter-

REHABILITATION INTERVENTIONS IN PARKINSON DISEASE

Table 1. Complementary Exercise Therapies

and Their Use in Parkinson Disease
Exercise

Definition

Alexander
Technique

A method of becoming more aware of simple

everyday movements that people of all ages
and abilities can learn to relieve the pain
and stress caused by everyday misuse of
the body.
Chinese massage that uses kneading,
pressing, rolling, shaking, and stretching of
the body. Tui-na is thought to regulate qi
(vital energy) and blood flow, and improve
the function of tendons, bones, and joints.
A form of traditional Chinese mind/body
exercise and meditation that uses slow and
precise body movements with controlled
breathing and mental focusing to improve
balance, flexibility, muscle strength, and
overall health.

Tui-na

Qigong

ventions [50-54]. The components of postural control and

balance that were measured in these studies included axiallycontrolled movements, dynamic posturography, compensatory stepping in response to external provocations and ability
to sustain tandem stance. The exercise interventions included upper and lower limb coordination and strengthening, spinal flexibility, postural correction, gait training, functional mobility training, external provocations on stable and
unstable surfaces, and endurance training. All observed outcomes were improved immediately after the intervention
phases of treatment, which ranged from 2 to 10 weeks
[50-54], and up to 2 months thereafter [53,54]. Sensory
cueing to enhance balance has not received as much investigation as gait in PD. One 3-week home-based program
resulted in small but significant improvement in posture and
timed performance during balance tests; however, functional
improvements were marginal, and the therapeutic effects of
cueing were not sustained 6 weeks later [55].

Complementary Exercise Treatments

Up to 40% of individuals who have PD use at least 1 type of
complementary treatment (Table 1); vitamins and herbs,
massage, and acupuncture are used most commonly. Twelve
percent are reported to have used 5 or more of these therapies. These estimates are higher than what has been reported
for the general American population (about 30%); their use is
more common among those with PD who are younger at
onset, have higher levels of income and education, and take a
higher daily dose of dopamine equivalent [56]. Assessing
efficacy of complementary exercise treatments to treat PD has
received little rigorous study. The immediate improvements
that were observed in 1 study after multi-modal spa therapy
(thermal baths, drinking mineral water, relaxation and exercise therapies) were not sustained 6 months later [57]. Stallibrass et al [58] compared the Alexander technique, massage
and no treatment during a nonblinded randomized clinical
trial over 12 weeks. The Alexander technique was relatively

PM&R

comparable to massage, and both were significantly better

than no treatment at stabilizing activity level. The study
subjects who were treated with the Alexander technique
qualitatively reported more improvements in posture, balance, gait, speech, and sitting ability, while those who were
treated with massage reported more often a relaxation effect
and a higher sense of well-being. Svircev et al [59,60]
compared neuromuscular massage and music relaxation
therapy in a clinical trial that compared subjects with PD
randomly assigned to each type of treatment. After twice
weekly treatments over 4 weeks, significant improvements in
clinical parkinsonian motor signs were observed in those
who received massage. An open trial [61] investigating use of
sequential tui-na massage, acupuncture, and qigong over 6
months in 25 subjects with PD found no objective improvement in measures of impairment and activity; however, subjective improvement was reported in 16 patients, and measures of quality of life and depression improved significantly.
Burini et al [62] in a randomized controlled crossover trial
comparing aerobic exercise and qigong in 26 subjects with
advanced PD found that aerobic training, but not qigong, had
significant impact on the ability of moderately disabled subjects to tolerate exercise. When exploring the use of exercise
and chemical supplementation, Hass et al [63] randomized
20 patients with PD to receive progressive resistive training
combined either with creatine monohydrate or placebo for
12 weeks. The former group demonstrated significantly
greater improvements in strength, particularly as measured
by their ability to arise from a chair.

Treatment of Upper Limb Motor

Control Deficits
Murphy and Tickle-Degnens review [64] of 16 studies involving OT-related interventions directed toward small samples of individuals who had PD was guardedly optimistic
regarding the outcomes after a variety of interventions. Several studies incorporated external cueing strategies. Platz et al
[65] studied the speed and accuracy of performing an upper
limb aiming task in bradykinetic-predominant individuals
who had PD. The tasks were performed under 2 training
conditions, aiming with and without an auditory cue. No
differences in improvements of performance speed between
the cued and noncued training conditions were observed.
Rogers et al [66] applied a serial 2-way reaction time task in
which advanced information (visual cue) about the next
movement was not provided until after the current movement was initiated. Their objective, thus, was to probe the
ability to use advanced information to guide movement.
When using the sequential sensory cues became a more exact
way to guide fine motor control, the subjects with PD displayed significantly slower movement compared to the control subjects. This finding suggests that attention to the cue
alone may not be adequate, and that perhaps what was
problematic in the subjects with PD was an inability to plan
motorically when provided more specific sensory information. Meshack et al [67] studied the therapeutic use of

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S45

weighted utensils and wrist cuffs as a compensatory strategy

in tremor-predominant individuals with PD. No differences
in modifying the amplitude or frequency of tremor were
observed. Studying the effects of visually-guided virtual reality training in 2 persons with PD, Albani et al [68] observed
their performance of 3 upper-limb functional activities.: The
use of virtual reality was viewed as successful; however, this
success did not translate into improved function in everyday
life.

Treatment of Hypokinetic Dysarthria

Critical reviews [69-71] of speech therapy interventions in
PD have concluded that evidence exists to support their
efficacy, but that evidence is equivocal. The best-studied
exercise-based treatment for hypokinetic dysarthria is the Lee
Silverman Voice Treatment (LSVT) program, which has
been reported as efficacious up to 24 months after treatment.
This therapy has 3 aims: (1) to increase strength and muscle
endurance of the respiratory muscles in order to overcome
rigid laryngeal muscles that create resistance to air flow and
hypophonia; (2) to facilitate more complete vocal cord adduction by increasing subglottal air pressure and vocal cord
vibration; and (3) to recalibrate the impaired internal sensory perception of the effort to speak that prevents accurate
self-monitoring of vocal output [72-77]. It also has 3 caveats:
it should be administered by a speech and language pathologist trained in LSVT; it requires a commitment to intensive
treatment for 50 minutes, 4 times weekly within a 1- month
time period; and it requires participation in daily homework during treatment and thereafter to maintain the observed gains from treatment. When directly compared to
therapy aimed only at enhancing vocal volume by facilitating
increased respiratory effort, LSVT is superior because it both
enhances vocal volume and facilitates vocal cord adduction
[73,74]. LSVT also has generalizability of observed improvements beyond vocal volume to include prosody, intelligibility, facial expression and swallowing [72,73,75]. Liotti
et al [76] reported changes in the brain, as seen in positron
emission tomography (PET) in 5 subjects with PD who had
been treated with LSVT. There was normalization, or decreased cerebral activation, in the left motor cortex and
concurrently increased activation in the right anterior insular
and dorsolateral prefrontal cortices and in the head of the
caudate and putamen of the basal ganglia.
Other treatments that incorporate some or all of the components of LSVT, such as Pitch Limiting Voice Treatment
(PLVT), have been promoted. This treatment, characterized
as speak loud and low treatment was developed because
LSVT (think loud, think shout) may be too effortful, resulting in highly pitched, strained, screaming vocal output.
The deSwart et al [78] researchers reported that PLVT has
comparable efficacy to LSVT, yet has the advantage of producing less pressured speech at more normal vocal frequencies [78].

S46

Moroz et al

REHABILITATION INTERVENTIONS IN PARKINSON DISEASE

CAREGIVER TRAINING

arthria, since speech therapy only aims at a single factor, that

of enhancing vocal volume by facilitating increased respiratory effort. Caregiver education may provide caregivers with
a greater sense of control and mitigate their depression. It is
not clear whether interventions can increase caregiver participation or reduce caregiver strain. Physiatrists must be familiar with the available modalities and the body of evidence
supporting the use of specific treatment approaches, while
balancing the ever incomplete data against the particular
needs of individual patients.

As the PD progresses, the increasing severity of cognitive

impairments appears fundamental to increasing the burden
of care [79]. The survey by Davey et al [80] of spousal
caregivers of recurrent fallers who had PD found that caregivers may have their own fear of falling syndrome regarding their vulnerable spouses, and they often injured themselves when helping their spouses arise from the floor. These
caregivers reported a lack of education about preventing falls.
They also were not knowledgeable about how to manage the
consequences of falls, such as minimizing potential injury to
themselves and their spouse as they assisted the faller back to
the upright position. Fernandez et al [81] explored the factors that underpin depression among spousal caregivers of
those with PD; longer disease duration was the strongest
predictor of caregiver depression.
Nursing researchers have investigated strategies that focus
mainly on cognitive-behavioral approaches aimed at counteracting caregiver depression. These approaches include
learning optimism; re-engaging with ones inner locus of
control to counteract a sense of being controlled by outer
forces; maintaining ones own life; encouraging the patientcaregiver dyad to stay active; and focusing on what is meaningful to the individual despite ongoing loss and frustration
in handling loss as the disease progresses [82-84]. Interventions facilitating participation in the caregiver role (for example, appropriate biomechanical methods to provide mobility
assistance) have not been studied. Nor have studies been
done on therapies aiming to reduce the risks of caregiver
strain in PD. This line of investigation has been explored in
patient-caregiver pairs among populations with Alzheimer
disease. For example, the OT-based caregiver training program of environmental skills building presented by Gitlin et
al [85] can serve as a model for caregiver training in PD.
In summary, new dopaminergic agents and deep brain
stimulation procedures are facilitating a longer period of
functional stability for individuals who have PD. Adjunctive
exercise-based treatments, thus, can be applied over longer
periods of time to optimize function before inevitable decline
from this neurodegenerative disease. Strong evidence exists
that external sensory cues are useful in the treatment of
locomotion deficits, including freezing of gait. Gait parameters, functional status and quality of life generally improve at
the end of treatment, but are not consistently sustained
thereafter. There is also strong evidence that targeted exercise
produces short-term improvement in postural control and
balance. While complementary treatment modalities are
used widely by patients with PD, only use of various massage
techniques seems to improve subjective well being and quality of life. Interventions based on occupational therapy techniques that use external cueing and are aimed at treating
upper limb motor control deficits have some efficacy. Use of
weighted utensils and visually based virtual reality does not
seem to affect tremor or function, respectively. Some evidence exists that techniques such as LSVT and PLVT are
superior to speech therapy for treatment of hypokinetic dys-

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