Rehabilitation Interventions in Parkinson Disease

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bjective: This self-directed learning module provides an evidence-based update ofxercise-based rehabilitation interventions to treat Parkinson disease (PD). It is part of thetudy guide on stroke and neurodegenerative disorders in the Self-Directed Physiatricducation Program for practitioners and trainees in physical medicine and rehabilitation.his focused review emphasizes treatment of locomotion deficits, upper limb motor controleficits, and hypokinetic dysarthria. New dopaminergic agents and deep brain stimulationre facilitating longer periods of functional stability for patients with PD. Adjunctivexercise-based treatments can therefore be applied over longer periods of time to optimizeunction before inevitable decline from this neurodegenerative disease. As function deteri-rates in patients with PD, the role of caregivers becomes more critical, thus trainingaregivers is of paramount importance to help maintain a safe environment and limitaregiver anxiety and depression. The overall goal of this article is to enhance the learner’sxisting practice techniques used to treat PD through exercise-based intervention methods.

NTRODUCTION

arkinson disease (PD) is a common aging-related neurodegenerative disease. Its cause isnknown; the pathophysiology has been explained by nigrostriatal pathway degenerationssociated with excessive accumulation of alpha-synuclein in specific areas of the brain [1].he vulnerable areas include the locus ceruleus, hypothalamus, cranial nerve motor nucleind autonomic nervous system [1]. The mainstay of treatment is dopaminergic replacementr enhancement. Despite the new agents that are continually being developed to augmentopamine availability in neural tissue, as many as 50% of individuals with PD becomeefractory to medical management beyond 5 years after initiation of treatment [2]. Thisefraction manifests as the patient experiencing rapid motor fluctuations and/or dyskinesiashen on medication. Over the last 10 years, physiologic ablative procedures to effect “deeprain stimulation” of specific nuclei of the basal ganglia (subthalamic, globus pallidus

nternus) have become viewed as efficacious for up to 75% of appropriately selectedndividuals who are considered medically refractory. The procedures are considered pallia-ive, and their efficacy has been defined by stabilized function and improved quality of lifep to 5 years after surgery. For some individuals, this stabilization allows time to incorporatexercise-based interventions as an adjunct to medical and surgical treatments. Thesenterventions can support functional stability before inevitable decline [3,4].

Several essential reviews of exercised-based interventions for persons with PD reportedavorable outcomes [5-8]. However, the literature is still evolving in that: (1) less than halff the reviewed studies were randomized controlled trials; (2) about one-third of theeviewed studies had sample sizes of fewer than 16 subjects; (3) more than half of theeviewed studies discontinued their observations at the completion of the interventionhases, not observing whether the positive effects of various interventions were sustainedver time. This present review provides an update of specific rehabilitation interventions inD supported by the literature.

ULTIDISCIPLINARY REHABILITATION INTERVENTIONS

unvisson et al [9] reported their observations of treatment that combined nursing educa-

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PM&R © 2009 by the American Academy of P1934-1482/09/$36.00

Printed in U.S.A.42

.M. NYU School of Medicine, Rusk Institutef Rehabilitation Medicine, New York, NY.ddress correspondence to: A.M.; e-mail:[email protected]: 2, IPRO

.R.E. University of Utah, Salt Lake City, UTisclosure: 2, Northstar Neuroscience

.L.L. Harvard Medical School, VA Bostonealthcare System, Physical Medicine andehabilitation Service, Boston, MAisclosure: nothing to disclose

.C. Case Western Reserve University, De-artment of Physical Medicine and Rehabili-

ation, MetroHealth Medical Center, Cleveland,Hisclosure: nothing to disclose

.A.L. Santa Clara Valley Medical Center, Sanose, CAisclosure: nothing to disclose

.C.R. Department of Physical Medicine andehabilitation, University of Pittsburgh Medicalenter, Pittsburgh, PAisclosure: nothing to disclose

.M.R. Department of Physical and Rehabili-ation, University of Pennsylvania Hospital,hiladelphia, PAisclosure: nothing to disclose

isclosure Key can be found on the Table ofontents and at www.pmrjournal.org

hysical Medicine and RehabilitationSuppl. 1, S42-S48, March 2009

DOI: 10.1016/j.pmrj.2009.01.018

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hich consisted of twice weekly 2-hour sessions over 5eeks — resulted in significant improvements in reported

elf-care, and in observed speed and integration of motorontrol. These results were seen at the end of the interventionhase and 3 months later. Moreover, significant improve-ents in quality of life (QOL) were observed 3 months after

he end of the intervention phase. The QOL improvementsere explained primarily by improved regulation of sleep-ake cycles. Trend et al [10] conducted an open trial of

ehabilitation interventions of 118 PD patient-caregiverairs. The interventions, conducted once weekly over 6eeks, encompassed a structured therapeutic day of 1-on-1

nd group sessions of PT, occupational therapies (OT) andpeech therapies (ST). The sessions were conducted as a dayospital program. Significant gains in gait, voice articulation,nd quality of life occurred during the first 6 weeks. How-ver, when the same interventions were later subjected to arossover design after randomization of another 71 patient-aregiver pairs, a different outcome was observed. The sameositive effects were not observed at the 6- month cross-overoint. At 6 months postintervention gait improvements ap-roached significance, but QOL deteriorated [11]. Moreover,here was an increase in caregiver strain that approachedignificance at this 6-month point. The difference in outcomeetween the 2 studies may be due to the mistiming of the

ntervention [12] or difference in rigor. Nieuwboer et al [13]rovided 2 guidelines to avoid “mistimed” application ofreatments. They found that (1) a higher disease severity isegatively predictive of therapeutic benefits even in the con-ext of a familiar home environment and (2) compromisedognitive ability and older age were negatively predictive ofbility to sustain the therapeutic benefits of treatment. Theseuides lead us to 2 conclusions. First, for older persons withD who are more cognitively impaired because their PD is ofigher severity, it is rational to focus rehabilitation efforts onaregiver training. Second, for persons in middle and latertage PD, it would appear rational to view the patient-care-iver pair as “the patient.”

REATMENT OF LOCOMOTION DEFICITS

hile critical reviews of PT interventions have been optimis-ic, many studies were methodologically flawed because ofheir small sample sizes, lack of randomization, and nonuni-ormity of interventions, reflecting a lack of recognized stan-ards of “best practice” [14-16].

xternal Sensory Cueing

he best studied exercise-based interventions to treat the gaitifficulties of PD are those that have used external sensoryueing strategies, including visual (spatial) and auditorytemporal) strategies [17]. Researchers doing gait analysestudies have found that persons with PD experience lessentral delivery of proprioceptive feedback and that 1 of thetrategies they use to compensate for that is an increased

ues are hypothesized to be a way for the person with PD tose available neural networks that are mediated through theerebellum as a therapeutic bypass strategy. Auditory cues,n the other hand, are hypothesized to be a therapeuticestorative strategy to replace externally the degeneratedasal ganglia’s “internal timekeeping” function [18,19]. Aeries of studies [20-28] on the use of compensatory sensoryystems to enhance mobility was explored in laboratory andlinical studies on gait. These studies compared outcomesuring non-cued and cued conditions, often comparing theerformances of subjects with PD and control subjects. Thepplied visual cues included floor stripes, timing lights andirrors; the auditory cues included music and metronomes.ait velocity and walking speed consistently, but not univer-

ally, improved during the cued conditions in those with PD.isual cues more frequently led to increased stride length,hile auditory cues were more frequently observed to in-

rease cadence [20-28]. Visual cues were more effective atmproving gait initiation than were auditory cues [29]. How-ver, the only studies reporting that these positive effects ofensory cues on gait can be sustained over longer periods ofime were case studies [30].

Dual task studies in which subjects performed cognitiver motor tasks while walking have been done [31]. In thesedual paradigm” studies the researchers’ intent was to “di-ide” the subjects’ attention between the tasks and the walk-ng action. In these studies subjects performed concurrentasks under cued gait training conditions. The findings fromhese studies indicate that external sensory cues fundamen-ally enhance attention to the alternative cue during ambula-ion. However, the hypothesis that giving one’s attention toxternal, rhythmic, auditory and visual cues will somehowither bypass or restore sensory control of movement is notupported [31]. Other investigators’ critiques of these sen-ory cueing studies reinforce that the fundamental deficit ofait problems in PD is attentional, and that any strategy thatnhances attention during walking will have an effect similaro that of sensory cues [32].

Other approaches that use alternative sensory stimulationo influence motor control are less demanding of attentionalesources. One randomized controlled crossover trial ofhole-body-vibration in 68 subjects with PD demonstrated

ignificant decline in clinical parkinsonian motor signs, par-icularly tremor and rigidity [33].

raditional Physical Therapies (PTs)

everal clinical trials have applied a variety of exercise inter-entions, comparing treatment and no-treatment groups, inubjects with PD and control subjects. Intervention phases ofreatment in these PT studies ranged from 1 to 20 weeks.

hen postintervention outcomes were observed, they weresually limited to less than 6 months after the end of the

ntervention phases. Outcome measurements included gaitarameters, functional status and quality of life, and wereenerally reported as improved at the end of the intervention

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34-38]. Several of the trials that applied novel treatmentsuch as partial body weight-supported treadmill training39,40], “polestriding” (walking with modified ski poles withmovement pattern similar to cross-country skiing) [41] andtructured treadmill training [42] found these strategies to beuperior to usual PT approaches for increasing gait velocitynd improving functional status. Dibble et al [43,44] studiedhe effects of strengthening in 19 PD patients randomized toccentric and concentric isometric strengthening groups,ho were given PT 3 days weekly over 12 weeks. In this

tudy eccentric strengthening was associated with greateruscular hypertrophy and better force generation and mo-

ility than concentric strengthening; when high-force eccen-ric strengthening was continued for 12 more weeks in aubset of 10 subjects during an open trial, no clinical oraboratory evidence of muscle damage was observed. Tamirt al [45] compared PT-guided motor imagery in combina-ion with exercise, and exercise alone, in a small-sample,andomized controlled trial. The combination treatment wasore effective for reducing parkinsonian motor signs, partic-larly bradykinesia.

reatment of Freezing of Gait

reezing of gait is reported to occur in up to 50% of individ-als who have PD. It is associated with higher disease severitynd longer disease progression [46]. Freezing of gait contin-es to be pathophysiologically elusive; however, it is wellescribed clinically to occur when the sensory/perceptualemands of the environment require that a new motor pro-ram be used in order to continue a rational sequence ofovement [47]. Demands that cause individuals to freeze

nclude gait initiation, turning, walking through doorways,r approaching a terminal object. Freezing of gait can beinimized by using assistive devices, such as wheeled walk-

rs, in combination with “sensory-motor tricks.” The devicesrovide consistent proprioceptive delivery and the “tricks”re actually behavioral strategies that can be taught to bothatient and caregivers. One such strategy helps overcome theeeling that one’s feet are “glued” to the ground. The personith PD is taught not to actively disconnect his/her “glued

eet” from the ground, but rather to allow the motor block toccur, momentarily relax, then re-initiate gait. During train-ng, the person with PD is taught to use a hip/knee hyperflex-on maneuver to step out and over an imagined or real visualue. The cue may be, for example, a self-triggered laser beamt ankle level generated from the wheeled walker or cane or aow physical barrier, such as a yardstick laid flat on the floor48,49]. Empirically, the presence of the sensory cue doesot appear to be as essential as using the proximal leg flexorso re-initiate gait.

reatment of Deficits in Postural Controlnd Balance

everal open clinical trials have focused on observing pos-

entions [50-54]. The components of postural control andalance that were measured in these studies included axially-ontrolled movements, dynamic posturography, compensa-ory stepping in response to external provocations and abilityo sustain tandem stance. The exercise interventions in-luded upper and lower limb coordination and strengthen-ng, spinal flexibility, postural correction, gait training, func-ional mobility training, external provocations on stable andnstable surfaces, and endurance training. All observed out-omes were improved immediately after the interventionhases of treatment, which ranged from 2 to 10 weeks50-54], and up to 2 months thereafter [53,54]. Sensoryueing to enhance balance has not received as much investi-ation as gait in PD. One 3-week home-based programesulted in small but significant improvement in posture andimed performance during balance tests; however, functionalmprovements were marginal, and the therapeutic effects ofueing were not sustained 6 weeks later [55].

omplementary Exercise Treatments

p to 40% of individuals who have PD use at least 1 type ofomplementary treatment (Table 1); vitamins and herbs,assage, and acupuncture are used most commonly. Twelveercent are reported to have used 5 or more of these thera-ies. These estimates are higher than what has been reportedor the general American population (about 30%); their use isore common among those with PD who are younger at

nset, have higher levels of income and education, and take aigher daily dose of dopamine equivalent [56]. Assessingfficacy of complementary exercise treatments to treat PD haseceived little rigorous study. The immediate improvementshat were observed in 1 study after multi-modal “spa therapy”thermal baths, drinking mineral water, relaxation and exer-ise therapies) were not sustained 6 months later [57]. Stal-ibrass et al [58] compared the Alexander technique, massagend no treatment during a nonblinded randomized clinical

able 1. Complementary Exercise Therapiesnd Their Use in Parkinson Disease

Exercise Definition

lexanderTechnique

A method of becoming more aware of simpleeveryday movements that people of all agesand abilities can learn to relieve the painand stress caused by everyday misuse ofthe body.

ui-na Chinese massage that uses kneading,pressing, rolling, shaking, and stretching ofthe body. Tui-na is thought to regulate qi(vital energy) and blood flow, and improvethe function of tendons, bones, and joints.

igong A form of traditional Chinese mind/bodyexercise and meditation that uses slow andprecise body movements with controlledbreathing and mental focusing to improvebalance, flexibility, muscle strength, andoverall health.

rial over 12 weeks. The Alexander technique was relatively

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omparable to massage, and both were significantly betterhan no treatment at stabilizing activity level. The studyubjects who were treated with the Alexander techniqueualitatively reported more improvements in posture, bal-nce, gait, speech, and sitting ability, while those who werereated with massage reported more often a relaxation effectnd a “higher sense of well-being.” Svircev et al [59,60]ompared neuromuscular massage and music relaxationherapy in a clinical trial that compared subjects with PDandomly assigned to each type of treatment. After twiceeekly treatments over 4 weeks, significant improvements in

linical parkinsonian motor signs were observed in thoseho received massage. An open trial [61] investigating use of

equential tui-na massage, acupuncture, and qigong over 6onths in 25 subjects with PD found no objective improve-ent in measures of impairment and activity; however, sub-

ective improvement was reported in 16 patients, and mea-ures of quality of life and depression improved significantly.urini et al [62] in a randomized controlled crossover trialomparing aerobic exercise and qigong in 26 subjects withdvanced PD found that aerobic training, but not qigong, hadignificant impact on the ability of moderately disabled sub-ects to tolerate exercise. When exploring the use of exercisend chemical supplementation, Hass et al [63] randomized0 patients with PD to receive progressive resistive trainingombined either with creatine monohydrate or placebo for2 weeks. The former group demonstrated significantlyreater improvements in strength, particularly as measuredy their ability to arise from a chair.

reatment of Upper Limb Motorontrol Deficits

urphy and Tickle-Degnen’s review [64] of 16 studies in-olving OT-related interventions directed toward small sam-les of individuals who had PD was guardedly optimisticegarding the outcomes after a variety of interventions. Sev-ral studies incorporated external cueing strategies. Platz et al65] studied the speed and accuracy of performing an upperimb aiming task in bradykinetic-predominant individualsho had PD. The tasks were performed under 2 training

onditions, aiming with and without an auditory cue. Noifferences in improvements of performance speed betweenhe cued and noncued training conditions were observed.ogers et al [66] applied a serial 2-way reaction time task inhich advanced information (visual cue) about the nextovement was not provided until after the current move-ent was initiated. Their objective, thus, was to probe the

bility to use advanced information to guide movement.hen using the sequential sensory cues became a more exactay to guide fine motor control, the subjects with PD dis-layed significantly slower movement compared to the con-rol subjects. This finding suggests that attention to the cuelone may not be adequate, and that perhaps what wasroblematic in the subjects with PD was an inability to planotorically when provided more specific sensory informa-

ion. Meshack et al [67] studied the therapeutic use of c

eighted utensils and wrist cuffs as a compensatory strategyn tremor-predominant individuals with PD. No differencesn modifying the amplitude or frequency of tremor werebserved. Studying the effects of visually-guided virtual real-ty training in 2 persons with PD, Albani et al [68] observedheir performance of 3 upper-limb functional activities.: These of virtual reality was viewed as successful; however, thisuccess did not translate into improved function in everydayife.

reatment of Hypokinetic Dysarthria

ritical reviews [69-71] of speech therapy interventions inD have concluded that evidence exists to support theirfficacy, but that evidence is equivocal. The best-studiedxercise-based treatment for hypokinetic dysarthria is the Leeilverman Voice Treatment (LSVT®) program, which haseen reported as efficacious up to 24 months after treatment.his therapy has 3 aims: (1) to increase strength and musclendurance of the respiratory muscles in order to overcomeigid laryngeal muscles that create resistance to air flow andypophonia; (2) to facilitate more complete vocal cord ad-uction by increasing subglottal air pressure and vocal cordibration; and (3) to “recalibrate” the impaired internal sen-ory perception of the effort to speak that prevents accurateelf-monitoring of vocal output [72-77]. It also has 3 caveats:t should be administered by a speech and language pathol-gist trained in LSVT; it requires a commitment to intensivereatment for 50 minutes, 4 times weekly within a 1- monthime period; and it requires participation in daily “home-ork” during treatment and thereafter to maintain the ob-

erved gains from treatment. When directly compared toherapy aimed only at enhancing vocal volume by facilitatingncreased respiratory effort, LSVT is superior because it bothnhances vocal volume and facilitates vocal cord adduction73,74]. LSVT also has “generalizability” of observed im-rovements beyond vocal volume to include prosody, intel-

igibility, facial expression and swallowing [72,73,75]. Liottit al [76] reported changes in the brain, as seen in positronmission tomography (PET) in 5 subjects with PD who hadeen treated with LSVT. There was “normalization,” or de-reased cerebral activation, in the left motor cortex andoncurrently increased activation in the right anterior insularnd dorsolateral prefrontal cortices and in the head of theaudate and putamen of the basal ganglia.

Other treatments that incorporate some or all of the com-onents of LSVT, such as Pitch Limiting Voice TreatmentPLVT), have been promoted. This treatment, characterizeds “speak loud and low” treatment was developed becauseSVT (“think loud, think shout”) may be too effortful, result-

ng in highly pitched, strained, “screaming” vocal output.he deSwart et al [78] researchers reported that PLVT hasomparable efficacy to LSVT, yet has the advantage of pro-ucing less pressured speech at more normal vocal frequen-

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AREGIVER TRAINING

s the PD progresses, the increasing severity of cognitivempairments appears fundamental to increasing the burdenf care [79]. The survey by Davey et al [80] of spousalaregivers of recurrent fallers who had PD found that care-ivers may have their own “fear of falling” syndrome regard-ng their vulnerable spouses, and they often injured them-elves when helping their spouses arise from the floor. Thesearegivers reported a lack of education about preventing falls.hey also were not knowledgeable about how to manage theonsequences of falls, such as minimizing potential injury tohemselves and their spouse as they assisted the faller back tohe upright position. Fernandez et al [81] explored the fac-ors that underpin depression among spousal caregivers ofhose with PD; longer disease duration was the strongestredictor of caregiver depression.

Nursing researchers have investigated strategies that focusainly on cognitive-behavioral approaches aimed at coun-

eracting caregiver depression. These approaches includelearning” optimism; re-engaging with one’s “inner locus ofontrol” to counteract a sense of being controlled by “outerorces;” maintaining one’s own life; encouraging the patient-aregiver dyad to stay active; and focusing on what is mean-ngful to the individual despite ongoing loss and frustrationn handling loss as the disease progresses [82-84]. Interven-ions facilitating participation in the caregiver role (for exam-le, appropriate biomechanical methods to provide mobilityssistance) have not been studied. Nor have studies beenone on therapies aiming to reduce the risks of caregiverstrain” in PD. This line of investigation has been explored inatient-caregiver pairs among populations with Alzheimerisease. For example, the OT-based caregiver training pro-ram of environmental skills building presented by Gitlin etl [85] can serve as a model for caregiver training in PD.

In summary, new dopaminergic agents and deep braintimulation procedures are facilitating a longer period ofunctional stability for individuals who have PD. Adjunctivexercise-based treatments, thus, can be applied over longereriods of time to optimize function before inevitable declinerom this neurodegenerative disease. Strong evidence existshat external sensory cues are useful in the treatment ofocomotion deficits, including freezing of gait. Gait parame-ers, functional status and quality of life generally improve athe end of treatment, but are not consistently sustainedhereafter. There is also strong evidence that targeted exerciseroduces short-term improvement in postural control andalance. While complementary treatment modalities aresed widely by patients with PD, only use of various massageechniques seems to improve subjective well being and qual-ty of life. Interventions based on occupational therapy tech-iques that use external cueing and are aimed at treatingpper limb motor control deficits have some efficacy. Use ofeighted utensils and visually based virtual reality does not

eem to affect tremor or function, respectively. Some evi-ence exists that techniques such as LSVT and PLVT are

rthria, since speech therapy only aims at a single factor, thatf enhancing vocal volume by facilitating increased respira-ory effort. Caregiver education may provide caregivers withgreater sense of control and mitigate their depression. It isot clear whether interventions can increase caregiver partic-

pation or reduce caregiver strain. Physiatrists must be famil-ar with the available modalities and the body of evidenceupporting the use of specific treatment approaches, whilealancing the ever incomplete data against the particulareeds of individual patients.

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