Parkinson PHYS THER

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doi: 10.2522/ptj.20110472Originally published online July 19, 2012

2012; 92:1395-1410.PHYS THER.KohrtRobert S. Schwartz, Pamela Mettler and Wendy M.

Margaret Schenkman, Deborah A. Hall, Anna E. Barn,Disease: A 16-Month Randomized Controlled TrialExercise for People in Early- or Mid-Stage Parkinson

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Exercise for People in Early- or Mid-Stage Parkinson Disease: A 16-MonthRandomized Controlled TrialMargaret Schenkman, Deborah A. Hall, Anna E. Baron, Robert S. Schwartz,Pamela Mettler, Wendy M. Kohrt

Background. Exercise confers short-term benefits for individuals with Parkinsondisease (PD).

Objective. The purpose of the study was to compare short- and long-term responsesamong 2 supervised exercise programs and a home-based control exercise program.

Design. The 16-month randomized controlled exercise intervention investigated 3exercise approaches: flexibility/balance/function exercise (FBF), supervised aerobicexercise (AE), and home-based exercise (control).

Setting. This study was conducted in outpatient clinics.

Patients. The participants were 121 individuals with PD (Hoehn & Yahr stages 13).

Interventions. The FBF program (individualized spinal and extremity flexibilityexercises followed by group balance/functional training) was supervised by a phys-ical therapist. The AE program (using a treadmill, bike, or elliptical trainer) wassupervised by an exercise trainer. Supervision was provided 3 days per week for 4months, and then monthly (16 months total). The control group participants exer-

cised at home using the National Parkinson FoundationFitness Countsprogram, with1 supervised, clinic-based group session per month.

Measurements. Outcomes, obtained by blinded assessors, were determined at4, 10, and 16 months. The primary outcome measures were overall physical function(Continuous ScalePhysical Functional Performance [CS-PFP]), balance (FunctionalReach Test [FRT]), and walking economy (oxygen uptake [mL/kg/min]). Secondaryoutcome measures were symptom severity (Unified Parkinsons Disease Rating Scale[UPDRS] activities of daily living [ADL] and motor subscales) and quality of life(39-item Parkinsons Disease Quality of Life Scale [PDQ-39]).

Results. Of the 121 participants, 86.8%, 82.6%, and 79.3% completed 4, 10, and 16months, respectively, of the intervention. At 4 months, improvement in CS-PFPscores was greater in the FBF group than in the control group (mean difference4.3,95% confidence interval [CI]1.2 to 7.3) and the AE group (mean difference3.1,

95% CI0.0 to 6.2). Balance was not different among groups at any time point.Walking economy improved in the AE group compared with the FBF group at 4months (mean difference1.2, 95% CI1.9 to 0.5), 10 months (mean differ-ence1.2, 95% CI1.9 to 0.5), and 16 months (mean difference1.7, 95%CI2.5 to 1.0). The only secondary outcome that showed significant differences

was UPDRS ADL subscale scores: the FBF group performed better than the controlgroup at 4 months (mean difference1.47, 95% CI2.79 to 0.15) and 16months (mean difference1.95, 95% CI3.84 to 0.08).

Limitations. Absence of a non-exercise control group was a limitation of the study.

Conclusions. Findings demonstrated overall functional benefits at 4 months inthe FBF group and improved walking economy (up to 16 months) in the AE group.

M. Schenkman, PT, PhD, FAPTA,Physical Therapy Program,Department of Physical Medicineand Rehabilitation, School ofMedicine, University of ColoradoAnschutz Medical Campus, Mail-stop C-244, 13121 E 17th Ave,ED II South, Room L283106,Aurora, CO 80045 (USA). Addressall correspondence to Dr Schenk-

man at: [email protected].

D.A. Hall, MD, PhD, Departmentof Neurology, Rush Medical Cen-ter, Chicago, Illinois.

A.E. Baron, PhD, Department ofBiostatistics and Informatics, Col-orado School of Public Health,University of Colorado AnschutzMedical Campus.

R.S. Schwartz, MD, Division ofGeriatric Medicine, School ofMedicine, University of Colorado

Anschutz Medical Campus.P. Mettler, BS, Department of Bio-statistics and Informatics, Colo-rado School of Public Health,University of Colorado AnschutzMedical Campus.

W.M. Kohrt, PhD, Division of Geri-atric Medicine, School of Medi-cine, University of ColoradoAnschutz Medical Campus.

[Schenkman M, Hall DA, BaronAE, et al. Exercise for people inearly- or mid-stage Parkinson dis-

ease: a 16-month randomizedcontrolled trial. Phys Ther.2012;92:13951410.]

2012 American Physical TherapyAssociation

Published Ahead of Print:July 19, 2012

Accepted: July 10, 2012Submitted: December 17, 2011

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Parkinson disease (PD) is achronic, progressive disorderaffecting about 1% of people

over age 60 years and an estimated4% of people over the age of 80 years

in industrialized countries,1

and isanticipated to affect 8 to 9 millionpeople worldwide by 2030.2 Tradi-tional management of PD has beenby pharmacology or surgery, orboth. Evidence from various exerciseapproaches311 demonstrates bene-fits of exercise in preserving aspectsof function and quality of life.1216

However, a Cochrane review of2001 noted that there is insufficientevidence to support or refute theefficacy of any given form of physio-

therapy over another in Parkinsonsdisease, further stating, Thereforea consensus must be found as tobest practice physiotherapy forParkinsons disease.17 Despite con-siderable efforts, there is not yet suf-ficient evidence. Furthermore, mostinterventions studied were relativelyshort-term, benefits were reportedimmediately after the intervention,and few authors reported postinter-

vention follow-up. Available post-

intervention data (typically at 1226weeks)15 suggest benefits are lostafter supervision is terminated. Withno strategies in place to facilitateongoing exercise, this finding is notsurprising because PD is chronicand progressive. Ongoing exercise islikely necessary to combat declinesin strength, flexibility, and balanceand their functional consequences.

A next important step is to compare

interventions, not just in terms ofimmediate benefits, but also in termsof long-term outcomes. The program

with the greatest short-term benefitsafter supervised exercise may not

be the program with greatest bene-fits over the long term. Thus, thisinvestigation was designed to com-pare short- and long-term effects of2 supervised exercise programs with

those of a control program.

The 3 exercise approaches investi-gated were: (1) a flexibility/balance/function program (FBF) specificallydesigned for people with PD; (2) astandard aerobic endurance program(AE); and (3) as the control, a home-based program of exercises recom-mended by the National ParkinsonFoundation.18 The FBF and AE pro-grams were supervised 3 times a

week for 4 months, with tapered

supervision for 1 month, and thenonce monthly to 16 months. Thecontrol program was supervisedonce a month for 16 months.

The FBF intervention was based onexercises used in a previous investi-gation demonstrating improvementof spinal flexibility and balance inpeople with PD.8 That program wasenriched with exercises designedto enhance postural control and

overall function.19 At 4 months, weexpected to see the greatest benefits

with this program compared withthe other 2 programs. However, we

were concerned that participantscould have difficulty adhering to thisprogram once supervised interven-tion was completed.

Endurance exercise has knownhealth benefits20 and potentiallycould benefit people with PD.

Improved endurance could lead toimprovements in overall function, inparticular for those functions thatrequire endurance. We did not antic-ipate that endurance exercise wouldbe as successful in improving thosefunctional activities that requireflexibility and balance as wouldPD-specific exercises. However,long-term adherence might be easier

with this exercise regimen. Hence at10 and 16 months, it was possible

that participants in the AE groupwould perform better than those inthe FBF group.

The exercises outlined in Fitness

Counts,18

developed by the NationalParkinson Foundation, were chosenas a control because these exercisesare commonly given to patients bytheir neurologists without specificsupervision or follow-up. Because ofthe limited supervision, we antici-pated that this program would beless successful than the supervisedexercise programs in improving alloutcome measures.

Because of the degenerative nature

of PD, long-term exercise habits areessential; otherwise, the participantis likely to quickly lose any gainsachieved. Yet within 3 months to a

year, only 50% or fewer of individu-als with a variety of conditions stilladhere to an exercise program.21,22

Barriers to exercise have been exam-ined2326 and include poor exerciseself-efficacy, poor sense of controlover exercise behaviors, unfavorableself-concept, failure to exercise in

the past, insufficient knowledge andskill, and anxiety. Among factorsrelated to exercise adherence,2731

perhaps most important is readinessor willingness to change.32,33 Basedon theoretical constructs, investiga-tors have developed approaches forassisting individuals to develop regu-lar exercise habits.21,23,3436 Theseconstructs were instrumental indeveloping the current investigation.

In summary, this investigation com-pared 2 supervised exercise pro-grams and a control exercise pro-gram, both in the short term (4months) and the long term (10 and16 months). Strategies were in placeto enhance long-term adherence fol-lowing the supervised period ofexercise. Comparisons were made at4, 10, and 16 months, with the pri-mary endpoints at 4 and 10 months.Ourprimary hypotheses were:

Available WithThis Article atptjournal.apta.org

eTable: Exercise Interventions

Exercise for People in Early- or Mid-Stage Parkinson Disease

1396 f Physical Therapy Volume 92 Number 11 November 2012

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1. Overall function: The FBF and AEgroups would each have greaterimprovement on the ContinuousScalePhysical Functional Per-formance Test (CS-PFP) com-

pared with the control group.This hypothesis was based on theexpectation that both improvedflexibility and balance andimproved endurance would trans-late to improvements in func-tional ability.

2. Balance: The FBF group wouldhave greater improvement on theFunctional Reach Test (FRT) com-pared with the other groups. Thishypothesis was based on findings

from our prior investigation.8

3. Movement efficiency: The FBFgroup would have better econ-omy of walking than the othergroups. The causes of reducedeconomy of walking in people

with PD are unknown; however,we theorized that improved tho-racic flexibility from the FBF pro-gram might result in improved

walking economy.

Our secondary hypotheses were:

1. The FBF and AE groups wouldeach perform better than the con-trol group on the activities ofdaily living (ADL) and motor sub-scales of the Unified ParkinsonsDisease Rating Scale (UPDRS)because of the impact of these 2exercise programs on function.

2. At 4 months, the FBF and AEgroups would perform better onthe 39-item Parkinsons DiseaseQuestionnaire (PDQ-39) qualityof life scale because of the super-

vised exercise being performed 3times a week.

MethodStudy DesignThis was a randomized controlledexercise study for people with early-

or mid-stage PD. Participants wereenrolled between August 2003 and

April 2009; the last participantsreached 16 months in July 2010.

Participants were randomly assignedto 1 of 3 groups: (1) supervisedflexibility/balance/function exercise(FBF), (2) supervised aerobic exer-cise (AE), and (3) home exercise(control). Primary outcome mea-sures were: physical function as mea-sured by the CS-PFP,37 balance asmeasured by the FRT,38 and walkingeconomy (energy cost of walking, oroxygen uptake [VO2] in mL/min/kg).39 Secondary outcome measures

were: UPDRS ADL and motor sub-

scales and a measure of quality of life(PDQ-39).40 Endpoints were at 4months (the end of the supervisedexercise period for the AE and FBFgroups), 10 months, and 16 months.

Primary endpoints were at 4 and10 months.

This investigation was designed withsample sizes sufficient to detect clin-

ically important differences amonggroups on several relevant outcomemeasures. Initial sample size esti-mates (PASS software, NCSS LLC,Kaysville, Utah)41 were based onreported mean changes and standarddeviations of measures investigatedin the previous exercise interventionstudy utilizing a similar program,8 as

well as other change scores availableat the time of the grant submission.Included were FRT and functionalaxial rotation,8 CS-PFP,37 and UPDRS

(total and motor and ADL subscale)scores.42 Approximately halfwaythrough study accrual, updatedinformation on effect sizes for theCS-PFP, UPDRS, and FRT was used to

The Bottom Line

What do we already know about this topic?

Exercise benefits people who are in the early and middle stages ofParkinson disease (PD); however, there is insufficient evidence to deter-

mine the best approach. This investigation compared short-term and

long-term effects of 2 supervised exercise programs (a PD-specific pro-

gram and an endurance exercise program) to a control program, recog-

nizing that the program with the greatest short-termbenefits after super-

vised exercise may not be the program with the greatest long-term

benefits.

What new information does this study offer?

The findings from this study indicate that the PD-specific and endurance

programs confer different benefits, with the endurance program havingthe greatest long-term benefits. Clinicians can extrapolate from these data

to determine appropriate exercise programs for individual patients.

If youre a patient, what might these findings meanfor you?

For people with early- or mid-stage PD, different types of exercises

provide different short-term and long-term benefits. The greatest long-

term benefits may result from endurance training with monthly follow-up

visits.



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Contacted(N=811)

Consented and Scheduled forNeurological Screening

(n=162)

649Not eligible oruninterested at phone contact

9Not eligible due to failedneurological screening

Scheduled for BloodScreening(n=153)

Scheduled for ExerciseStress Test(n=138)

Randomized(n=121)

6Blood test failures4Withdrawals4Screened out due to other health issues1Deceased

9Failed exercise stress test8Withdrew

FBF Group(n=39)

Site 1: 28, Site 2: 9, Site 3: 2

Control Group(n=41)

Site 1: 31, Site 2: 8, Site 3: 2

AE Group(n=41)

Site 1: 31, Site 2: 10, Site 3: 0

2Personal issues1Health problems

Completed 4-mo Treatment(n=36)






2Missed appointment2Health problems1Moved1Deceased1Not happy with program

3Not happy with program1Did not return calls1Unable to commit the time1Missed appointment

2Health problems2Missed appointment2Health problems

1Health problems1Not happy with program

1Personal issues1Health problems

1Health problems1Unable to commit the time1Had deep brain stimulation1Health problems




Completed Program(n=96)

Figure 1.CONSORT diagram of flow of participants in the study. The control group participated in a home-based program of exercisesrecommended by the National Parkinson Foundation,18 the AE group participated in a standard aerobic endurance program, andthe FBF group participated in a flexibility/balance/function program specifically designed for people with Parkinson disease. Not allparticipants completed all of the time points, resulting in some fluctuating numbers in the flow diagram; this fluctuation was takencare of by the analysis approach.





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an hour south or 45 minutes north-west of Denver. All personnelwho supervised the exercise ses-sions were trained by the primaryinvestigator (M.S.), received written

materials outlining the exercise pro-tocols in detail,19,5255 and co-treatedwith the primary investigator period-ically to ensure consistency whenimplementing exercise protocols.

Individuals assigned to the FBF andAE groups participated in supervisedexercise 3 days a week for 4 months.In month 5, supervision was tapered(described below). Thereafter, par-ticipants were asked to participate ina supervised exercise session once a

month. The control group partici-pants exercised under supervisionduring an initial individual sessionand then once a month for 16months. All participants wereencouraged to perform their pre-scribed exercise program a total of5 to 7 days a week throughout the16 months.

The supervised FBF program con-sisted of 2 months of flexibility train-

ing one-on-one with a physical ther-apist,52,53 followed by 2 months ofsmall-group exercise (up to 6 partic-ipants) that included flexibility, bal-ance, and functional exercises.19

Supervised AE sessions included 5 to10 minutes of warm-up, 30 minutesof exercise at 65% to 80% of HRmax,and 5 to 10 minutes of cool-down.6

Participants were encouraged to usea treadmill, but were permitted touse a stationary bicycle or elliptical

trainer. All except 1 of the partici-pants performed at least some oftheir exercise on the treadmill. Thecontrol program consisted of exer-cises in the home setting utilizing

Fitness Counts, with a singlemonthly group exercise sessionsupervised by a physical therapist.Details of the exercises are pre-sented in the eTable (available atptjournal.apta.org).

All participants, regardless of groupassignment, were assisted in devel-oping long-term exercise habits.55

After randomization and beforebeginning to exercise, participants

met with their trainer to discussmotivation to exercise, potential bar-riers, and strategies to develop exer-cise habits. Participants were askedto record supervised and home exer-cise throughout 16 months. After 4months, to transition participants tounsupervised exercise, supervisionfor FBF and AE was tapered (2 ses-sions a week for 2 weeks, then 1session a week for 2 weeks). Every-one participated in a monthly exer-cise session, exercise diaries were

reviewed monthly, and strategieswere suggested to enhance adher-ence. Inquiry about adverse events

was made at these sessions but couldbe reported by participants at anytime.

Data AnalysisDescriptive analysis included means,standard deviations, and proportionsby group at baseline. Comparisonsacross the treatment groups for cat-

egorical variables were made usingchi-square tests or their exact coun-terparts, depending on expected val-ues. Continuous measures or scales

were compared using ANOVA. A lin-ear mixed model with main effectsfor endpoint (baseline and 4, 10, and16 months), the stratification vari-able used in randomization (sex),interaction terms between exercisegroup and endpoint, and levodopaequivalent dose as a time-varying

covariate was used to estimate theintervention effect at each timepoint for each dependent variable.For walking economy, after deter-mining that the VO2 treadmillspeed relationship was linear acrossmeasured walking speeds of 0.8 to3.5 mph, we modeled VO2as a func-tion of treadmill speed using a linearmixed model with a random inter-cept and slope. The other factors inthe mixed model for walking econ-

omy were the same as above, withthe addition of an endpoint speedinteraction and a group end-point speed interaction. For all ofthe mixed models, it was assumed

that the group means at baselinewere equal due to randomization,generally a more powerful approachfor longitudinal data analysis of a ran-domized clinical trial that is recom-mended for routine application byFitzmaurice et al.56All analyses weredone on an intention-to-treat basis.

Model fit was assessed using 2 loglikelihood and its associated chi-square test statistic. Interventioneffects on the primary outcomes at

4 and 10 months are the principalfocus of this report, but differencesat the end of the study period (16months) also were of interest. Effectsizes based on differences betweengroup means and 95% confidenceintervals (CIs) are reported along

with statistical significance (2-sidedPvalues). All statistical analysis wasperformed using SAS/BASE and SAS/STAT software, version 9.2 of theSAS System for Windows (SAS Insti-

tute Inc, Cary, North Carolina).57

Assessment of NonignorableMissingnessOverall, 94 (78%) of the participantshad complete data on the primaryoutcome measures. The analysesassume data are missing at random.

Analysis of plots of group meansover time stratified by the time ofthe last test completed58 indicatedthe findings were not biased by miss-

ing data (results not shown).

Role of the Funding SourceThis work was supported by grantsfrom the National Institutes ofHealth (R01 HD043770-04, ColoradoCTSI TL1 RR025778, P30 DK048520,and NS052487) and the ParkinsonsDisease Foundation.



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ResultsParticipants were 121 people inHoehn and Yahr stages 1 through 3;almost half were in stage 2. Themajority were men, married, retired,

and with an annual income of morethan $50,000. There were no statis-tically significant differences amongthe 3 groups for any demographicmeasures (Tab. 1). Retention washigh at 4 months (86.8%), 10 months(82.6%), and 16 months (79.3%)(Fig. 1), at least 10% higher overallthan planned for in our sample sizecalculations.

Table 2 includes the adjusted meansfrom the mixed model for each

group at each measurement timepoint. In Table 3, we present thedifferences between pairs of groupsin mean change from baseline. Foreach group and each outcome, meanchange was obtained through themodel regression estimates as theadjusted group mean at a giventime point minus the adjusted meanat baseline. Differences betweengroups in change from baseline wereobtained using contrasts (subtrac-

tion) of the model regression coeffi-cients. The results presented inTable 3 are reported below as thedifferences, with 95% CI, in meanchange from baseline between spe-cific pairs of exercise groups at agiven follow-up point.

As hypothesized with respect tooverall function, at 4 months the FBFgroup improved on the CS-PFP morethan the control group (mean differ-

ence

4.3, 95% CI

1.2 to 7.3) andmore than the AE group (mean dif-ference3.1, 95% CI0.0 to 6.2).Contrary to our hypothesis, the AEgroup did not improve more thanthe control group (mean differ-ence1.2, 95% CI2.0 to 4.3) onthe CS-PFP. However, at 10 and 16months, there were no differencesbetween any groups for CS-PFP.There were no differences in FRTscores at any time point (Tab. 3), in

contrast to our hypotheses. Also incontrast to the hypotheses, at 4months, walking economy (ie,reduced energy cost of walking)improved more in the AE group than

in the FBF group (mean differ-ence1.2 mL/kg/min, 95% CI1.9 to0.5) (Fig. 2). At 10 months,the difference between the AE andFBF groups persisted: the AE grouphad greater improvements in walk-ing economy than the FBF group(mean difference1.21 mL/kg/min, 95% CI1.92 to 0.49). At16 months, the AE group improvedmore on walking economy than thecontrol group (mean differ-ence1.3 mL/kg/min, 95% CI2.0 to 0.6) and the FBF group(mean difference1.7 mL/kg/min,95% CI2.5 to 1.0).

With regard to secondary outcomes,there were no group differences inthe change in PDQ-39 or UPDRSmotor subscale scores at any timepoint. We had hypothesized thatboth the FBF and AE groups wouldperform better than the controlgroup on the UPDRS ADL subscale,

but only the FBF group performedbetter than the control group at 4months (mean difference1.47,95% CI2.79 to 0.15) and at 16months (mean difference1.95,95% CI3.84 to 0.08).

Overall group time interactionsare shown in Table 4. Slope ofchange across the 4 time endpoints

was estimated using the regressionestimates for each outcome. The AE

and FBF groups demonstratedgreater improvements on the UPDRSADL subscale compared with thecontrol group (for each comparison:slope of0.2, 95% CI0.4 to 0.0).The FBF group demonstrated morefavorable effects on the CS-PFP thanthe control group (slope of 0.4, 95%CI0.0 to 0.8).

Five study-related non-seriousadverse events were reported: 3 non-

injurious falls (1 in each group) and 2reports of soreness or pain (both inthe AE group). Additionally, 24 non-serious adverse events (not duringexercise) were possibly related to

the study (2 sprain/strain: 1 in theFBF group and 1 in the AE group; 22soreness/pain: 9 in the FBF group, 9in the AE group, and 4 in the controlgroup). One participant died unex-pectedly after enrollment but beforerandomization.

DiscussionThis study examined both short-term(4-month) and long-term (10- and16-month) benefits of exercise forpeople with early- or mid-stage PD.

We embarked on this investigationto determine whether FBF, an exer-cise program targeted to people

with PD, would confer greater ben-efits than would AE, a general condi-tioning program, or a control pro-gram, and importantly to determine

whether the hypothesized differ-ences would persist over the longterm after completion of supervisedexercise 3 times a week. Study pro-cedures were designed to help par-

ticipants maintain benefits of exer-cise once the supervised portion ofthe study was completed. Immedi-ately following the supervised exer-cise period (4 months), the FBF pro-gram was superior to both the AEand control programs for improvingoverall function. However, the AEprogram was superior at 4, 10, and16 months for improving economyof walking.

Overall FunctionThe hypothesis that the FBF programwould generate better improve-ments in physical function than thecontrol program was based on find-ings from a previous 10-week studyof flexibility exercises compared to

wait-listed controls8 in which exer-cise improved both flexibility andFRT scores. We believed the pro-gram, augmented with balance andfunctional training, would improve



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Table 1.Baseline Characteristicsa

Variable

Group

P

Control

(n41)

AE

(n41)

FBF

(n39)

n (%)

Sex

.980bMale 26 (63.4) 26 (63.4) 24 (61.5)

Female 15 (36.6) 15 (36.6) 15 (38.5)

Race

.189c

American Native 1 (2.4) 0 0

Asian/Pacific Islander 0 0 2 (5.1)

African American 1 (2.4) 0 0

Caucasian 38 (92.7) 40 (97.6) 37 (94.9)

Hispanic 1 (2.4) 0 0

Other 0 1 (2.4) 0

Assistive device

.899c

Walker 1 (2.4) 2 (5) 0

Straight cane 3 (7.3) 3 (7.5) 4 (10.5)

Other 2 (4.9) 1 (2.5) 1 (2.6)

None 35 (85.4) 34 (85) 33 (86.9)

Community type

.464c

Rural 2 (4.9) 3 (7.5) 3 (7.9)

Medium (2,50050,000) 4 (9.8) 4 (10) 2 (5.3)

Large city (50,000) 13 (31.7) 21 (52.5) 16 (42.1)

Suburb 22 (53.6) 12 (30) 17 (44.7)

Living status

.285bAlone 4 (9.8) 2 (5) 6 (15.8)

With spouse, relative, or friend 37 (90.2) 38 (95) 32 (84.2)

Marital status

.555cMarried 35 (85.4) 36 (90) 29 (76.3)

Widowed 2 (4.9) 0 1 (2.6)

Divorced/separated 3 (7.3) 3 (7.5) 5 (13.2)

Work status

.134c

Retired 24 (58.5) 22 (55) 23 (60.5)

Keeping house 2 (4.9) 1 (2.5) 1 (2.6)

Not employed 1 (2.4) 1 (2.5) 6 (15.8)

Employed 14 (34.2) 16 (40) 8 (21.1)

Income

.358c$20,000/y 0 (0) 2 (5.9) 3 (8.6)

$20,001$50,000/y 11 (31.4) 6 (17.6) 9 (25.7)

$50,000/y 24 (68.6) 26 (76.5) 23 (65.7)

(Continued)





10/18

overall functional ability, and,

indeed, it did. The mean changefrom baseline of more than 6 pointssuggests that the FBF program con-ferred substantial functional bene-fits, possibly because of the globalnature of the functional training.This change is of particular clinicalsignificance, given that participantsin this study were nearing the thresh-old for disability, as evidenced bytheir low mean CS-PFP scores.59

However, the difference was not

maintained at 10 and 16 months,

possibly because participants werenot able to adhere sufficiently to thisprogram.

We hypothesized that the AE groupparticipants also would performbetter than controls on the CS-PFPbecause this continuous functionaltask requires endurance. However,this was not the case, suggesting thatendurance training alone is insuffi-cient for improving overall daily

function. This finding has important

ramifications when designing exer-cise programs for people with early-and mid-stage PD.

BalanceWe anticipated that the FBF groupparticipants would perform betteron the FRT, based on the prior inves-tigation utilizing the axial mobilityexercise program,8 but they did not.Possibly lack of significant improve-ment in the present investigation

Table 1.Continued

Variable

Group

P

Control

(n41)

AE

(n41)

FBF

(n39)

n (%)

Modified Hoehn & Yahr score

.836c

1 0 (0) 2 (4.9) 0 (0)

1.5 2 (4.9) 1 (2.4) 1 (2.6)

2 20 (48.8) 21 (51.2) 21 (53.8)

2.5 15 (36.6) 13 (31.7) 13 (33.3)

3 4 (9.8) 4 (9.8) 4 (10.3)

Variable

Group

P

Control

(n41)

AE

(n41)

FBF

(n39)

X (SD)

Modified Hoehn & Yahr score 2.3 (0.4) 2.2 (0.5) 2.3 (0.4) .724d

Age (y) 66.3 (10.1) 63.4 (11.2) 64.5 (10.0) .467d

Education 16 (3.2) 15.9 (3.4) 15.8 (2.9) .978d

Years diagnosed with PD at enrollment 4.5 (3.8) 3.9 (4.2) 4.9 (3.7) .537d

Folstein Mini-Mental Score 28.8 (1.5) 28.3 (1.8) 28.8 (1.1) .215d

UPDRS ADL subscale score 9.6 (4.8) 8.5 (4.8) 9.4 (4.9) .544d

UPDRS motor subscale score 25.9 (8.9) 24.4 (9.1) 24.3 (10.5) .717d

UPDRS total score 37.5 (13.7) 34.6 (13.0) 35.5 (13.9) .621d

CS-PFP score

Total 44.6 (15.9) 49.6 (15.4) 48.9 (17.2) .320d

FRT score (in) 12.5 (3.1) 13.6 (3.1) 12.9 (3) .266d

Resting V O2(mL/kg/min) 3.4 (0.6) 3.6 (0.6) 3.5 (0.9) .518d

PDQ-39 score 21.5 (9.6) 18.5 (13) 23.2 (13.6) .176d

a The control group participated in a home-based program of exercises recommended by the National Parkinson Foundation, 18 the AE group participated ina standard aerobic endurance program, and the FBF group participated in a flexibility/balance/function program specifically designed for people withParkinson disease (PD). Subtotals less than the total number of participants indicate some data were not provided by the participants. UPDRSUnitedParkinsons Disease Rating Scale, ADLactivities of daily living, CS-PFPContinuous ScalePhysical Functional Performance Test; FRTFunctional Reach Test,

V O2oxygen uptake, PDQ-3939-item Parkinsons Disease Questionnaire.b Pvalue from chi-square test.c Exact chi-squarePvalue.d Pvalue from analysis of variance.





11/18

reflected the relatively high func-tional reach distances at baseline. Ofimportance, even at 16 months themean FRT score was not less thanat baseline for any of the 3 groups,suggesting that all groups mighthave benefited to some extent withrespect to balance.

Movement Efficiency

We postulated that people with PDmight require more VO2 (hencereduced walking economy) becauseof the energy expenditure to over-come the overall stiffness associated

with PD. The FBF group did notimprove, but the AE group improvedsignificantly and substantially at all 3time points.

The finding that the AE programimproved walking economy was

unexpected. Energy cost of walking,when normalized to body weight, isrelatively unaffected by factors suchas sex and level of fitness (eg, obe-sity)60 and was not expected tochange in response to enduranceexercise training. Baseline data fromthe current study demonstratedabnormally low walking economy(higher energy cost) in patients with

PD compared with a control groupof people who were healthy.39 Thus,to understand why walking econ-omy improved in response to the

AE program, it will be necessary toinvestigate the mechanisms forimpaired walking economy associ-ated with PD. Several possibilitiesinclude39,61,62: (1) increased restingenergy expenditure, possibly associ-ated with tremors, although thisexplanation did not explain our

observed differences betweenpatients and controls; (2) impairedefficiency of mitochondrial energyproduction via oxidative phosphory-lation; (3) energy cost of ventilation,

which has been reported to beincreased in patients with PD; and(4) impaired mechanical muscle con-traction efficiency, which may beinfluenced by such factors as muscle

fiber type and multi-segment move-ment coordination. Centrally medi-ated mechanisms of reduced muscleforce production associated withPD63 also might contribute to theincreased energy demand.

The reduced economy of movementat baseline in our participants withPD, compared with individuals with-out PD,39 raises the possibility thatreduced economy of movement con-

Table 2.Linear ModelBased Meansa

Measure

Baseline 4 Months 10 Months 16 Months

All

Groups

(N

121)X (SE)

Control

Group

(n

35)X (SE)

AE

Group

(n

34)X (SE)

FBF

Group

(n

36)X (SE)

Control

Group

(n

33)X (SE)

AE

Group

(n

32)X (SE)

FBF

Group

(n

34)X (SE)

Control

Group

(n

31)X (SE)

AE

Group

(n

31)X (SE)

FBF

Group

(n

33)X (SE)

CS-PFP score

(higher is better)

Total 48.8 (1.9) 50.7 (2.1) 51.9 (2.2) 55.0 (2.1) 51.1 (2.4) 51.3 (2.4) 50.3 (2.3) 49.6 (2.4) 50.5 (2.4) 52.9 (2.4)

FRT score (in)

(higher is better)

Forward 13.3 (0.4) 13.7 (0.5) 14.0 (0.5) 13.4 (0.5) 13.6 (0.5) 13.4 (0.5) 13.2 (0.5) 13.4 (0.5) 13.8 (0.5) 13.6 (0.5)

UPDRS score

(lower is better)

ADL 8.1 (0.6) 9.1 (0.7) 7.8 (0.7) 7.6 (0.7) 9.2 (0.8) 7.5 (0.8) 8.4 (0.8) 9.5 (0.8) 7.8 (0.8) 7.6 (0.8)

Motor 23.7 (1.2) 23.8 (1.5) 21.8 (1.5) 23.6 (1.5) 24.4 (1.5) 22.9 (1.6) 23.7 (1.5) 24.2 (1.8) 21.9 (1.8) 23.7 (1.7)

Total 33.3 (1.6) 34.4 (1.9) 30.8 (2.0) 32.5 (1.9) 35.7 (2.2) 32.1 (2.2) 33.9 (2.2) 35.6 (2.4) 31.4 (2.4) 32.6 (2.4)V O2(mL/kg/min)

(lower is better)

Intercept 5.2 (0.3) 5.6 (0.4) 4.5 (0.5) 5.6 (0.4) 4.9 (0.4) 4.4 (0.5) 5.7 (0.4) 5.0 (0.4) 3.6 (0.5) 5.3 (0.5)

Adjusted slope 3.0 (0.1) 2.7 (0.2) 2.9 (0.2) 2.9 (0.2) 3.1 (0.2) 3.0 (0.2) 2.9 (0.2) 3.1 (0.2) 3.2 (0.2) 3.2 (0.2)

PDQ-39 score(lower is better)

Total 17.2 (1.5) 16.3 (1.8) 14.5 (1.8) 18.4 (1.8) 18.4 (2.0) 16.4 (2.0) 15.3 (1.9) 21.0 (2.2) 17.1 (2.3) 17.2 (2.1)

a The model likelihood ratio chi square .001 for all models. Models include the following design variables and covariate adjustments: sex (categorical, 2levels), time (categorical, 4 levels), group time interactions (6 dummy variables), levodopa equivalents (continuous). The control group participated in ahome-based program of exercises recommended by the National Parkinson Foundation,18 the AE group participated in a standard aerobic enduranceprogram, and the FBF group participated in a flexibility/balance/function program specifically designed for people with Parkinson disease (PD). UPDRSUnited Parkinsons Disease Rating Scale, ADLactivities of daily living, CS-PFPContinuous ScalePhysical Functional Performance Test, FRTFunctionalReach Test, V O2oxygen uptake, PDQ-3939-item Parkinsons Disease Questionnaire, SEstandard error.





12/18

Table

3.

EstimatedMeanDifferencesBetweenGroups(TreatmentEffect)a

Measure

A

EGroupvs

Co

ntrolGroup

FBFGroupvs

ControlGroup

AEGroupvs

FBFG

roup

AEandFBFG

roupsvs

ControlG

roup

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95

%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

Changeinmeansat4months

CS-PFPscore

Total

1.2(1.6)

2.0to4.3

.465

4.3(1.5)

1.2to7.3

.006

3.1(1.6)

6.2

to0.0

.048

2.7(1.3)

0.1

to5.4

.046

FRT Fo

rward

0.3(0.5)

0.6to1.2

.519

0.3(0.4)

1.2to0.6

.456

0.6(0.5)

0.3

to1.5

.168

0.0(0.4)

0.8

to0.8

.960

UPDRSscore

ADL

1.3(0.7)

2.6to0.1

.060

1.5(0.7)

2.8to0.2

.029

0.2(0.7)

1.2

to1.5

.794

1.4(0.6)

2.5

to0.2

.019

Motor

2.0(1.5)

5.0to1.0

.191

0.2(1.5)

3.2to2.7

.877

1.8(1.5)

4.8

to1.2

.244

1.1(1.3)

3.7

to1.5

.393

Total

3.6(1.8)

7.1to0.1

.042

1.9(1.7)

5.3to1.5

.279

1.7(1.7)

5.2

to1.7

.321

2.7(1.5)

5.7

to0.2

.071

VO2

(mL/kg/min)

Intercept

slope

1.0(0.3)

1.7to0.4

.002

0.2(0.3)

0.4to0.8

.544

1.2(0.4)

1.9

to0.5

.001

0.4(0.3)

0.9

to0.1

.122

PDQ-39score

Total

1.8(1.7)

5.2to1.6

.299

1.1(1.7)

4.5to2.3

.506

0.6(1.7)

4.0

to2.8

.707

1.5(1.5)

4.4

to1.5

.325


CS-PFPscore

Total

0.3(2.0)

3.8to4.3

.892

0.7(2.0)

4.7to3.3

.722

1.0(2.0)

3.0

to5.0

.624

0.2(1.8)

3.7

to3.3

.901

FRT Fo

rward

0.2(0.6)

1.3to0.9

.714

0.4(0.6)

1.5to0.7

.453

0.2(0.6)

0.9

to1.3

.706

0.3(0.4)

1.2

to0.6

.456

UPDRSscore

ADL

1.7(0.9)

3.5to0.2

.083

0.8(0.9)

2.7to1.0

.373

0.8(0.9)

2.7

to1.0

.382

1.2(0.8)

2.9

to0.4

.129

Motor

1.6(1.7)

4.9to1.8

.353

0.8(1.6)

4.0to2.5

.648

0.8(1.7)

4.1

to2.5

.625

1.2(1.4)

4.0

to1.7

.422

Total

3.7(2.3)

8.2to0.9

.111

1.9(2.2)

6.3to2.6

.407

1.8(2.3)

6.3

to2.7

.426

2.8(2.0)

6.7

to1.1

.160

VO2

(mL/kg/min)

Intercept

slope

0.6(0.3)

1.3to0.1

.079

0.6(0.3)

0.0to1.2

.069

1.2(0.4)

1.9

to0.5

.001

0.0(0.3)

0.6

to0.5

.972

PDQ-39score

Total

2.0(2.1)

6.1to2.1

.340

3.1(2.0)

7.2to0.9

.128

1.2(2.1)

3.0

to5.3

.577

2.6(1.8)

6.1

to1.0

.153

(Continued)





13/18

tributes to the fatigue experiencedby many individuals with PD.64 Wedid not specifically measure fatigue,but this possibility should be consid-ered in future investigations of aero-

bic conditioning.

Secondary OutcomesThe FBF group had significantly bet-ter performance on the UDPRS ADLsubscale at both 4 and 16 months.However, the UPDRS ADL change

was small and of questionable clini-cal significance. No other group dif-ferences were found. Possibly all par-ticipants continued to be active andto benefit from their respective inter-

ventions. This interpretation is sup-

ported by data from a subset of ourparticipants who participated in aqualitative study 1 year after com-pleting the 16-month parent study.65

Individuals from all 3 of the exercisegroups (FBF, AE, and control) indi-cated that they continued to exer-cise after completion of the study,although typically at a lower inten-sity than during the study.

All 3 treatment groups demonstrated

remarkably little change in UPDRSmotor subscale scores over 16months. Yet, based on the naturalhistory of PD, the expected rate ofincrease in the UPDRS motor sub-scale score in levodopa-treatedpatients (on-medication state)

would have been at least 2 to 3points per year.66 Lack of compara-ble decline in these data, as well ason other outcome measures, sup-ports the impression that all partici-

pants benefited to some degree fromtheir exercise. We also cannot ruleout the possibility of a placeboeffect, known to be powerful amongpeople with PD.67

Retention of 79.3% at 16 months sug-gests that long-term interventionstudies can be carried out success-fully in this population. Further-more, the low rate of adverse eventssuggests that patients with PD canT

able

3.

Continued

Measure

A

EGroupvs

ControlGroup

FBF

Groupvs

ControlGroup

AEGr

oupvs

FBFGroup

AEandFBFG

roupsvs

ControlG

roup

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95%

CI

P


CS-PFPscore

Total

0.9(2.0)

3.1to4.8

.660

3.3(1.9)

0.5to7.2

.091

2.4(2.0)

6.3to1.4

.216

2.1(1.7)

1.3to5.5

.221

FRTscore

Forward

0.4(0.5)

0.6to1.4

.442

0.3(0.5)

0.7to1.2

.616

0.1(0.5)

0.9to1.1

.777

0.3(0.4)

0.5to1.2

.463

UPDRSscore

ADL

1.7(1.0)

3.6to0.2

.078

1.9(0.9)

3.8to0.1

.041

0.2(0.9)

1.6to2.1

.805

1.8(0.8)

3.5to0.2

.029

Motor

2.3(1.8)

5.9to1.4

.217

0.5(1.8)

4.1to3.1

.774

1.8(1.8)

5.4to1.8

.331

1.4(1.6)

4.5to1.7

.376

Total

4.2(2.5)

9.1to0.7

.094

3.0(2.4)

7.8to1.8

.220

1.2(2.4)

6.1to3.6

.622

3.6(2.1)

7.8to0.6

.094

VO2

(mL/kg/min)

Intercept

slope

1.3(0.3)

2.0to0.6

.0001

0.4(0.3)

0.3to1.1

.230

1.7(0.4)

2.5to1

.0001

0.5(0.3)

1.0to0.1

.108

PDQ-39score

Total

3.9(2.5)

8.8to1.0

.114

3.8(2.3)

8.5to0.8

.102

0.1(2.4)

4.9to4.7

.975

3.9(2.1)

8.0to0.2

.064

a

Thecontrolgroupparticipatedinahome-basedprogramofexercisesrecommendedby

theNationalParkinsonFoundation,1

8

theAEgroupparticipatedinastandardaerobicenduran

ceprogram,and

theFBFgroupparticipatedinaflexibility/b

alance/functionprogramspecificallydesignedforpeoplewithParkinsondisease(PD).UPDRS

UnitedParkinsonsDiseaseRatingScale,ADLactivitiesofdaily

living,CS-PFPContinuousScalePhysicalFunctionalPerformanceTest,FRTFunctionalReachTest,VO2oxygenuptake,PDQ-3939-itemParkinsonsDiseaseQuestionnaire,SEstan

darderror,95%

CI95%confidenceinterval.



http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/http://ptjournal.apta.org/


14/18

engage in relatively vigorous tread-mill exercise. These findings con-trast with data from a small pilotstudy, indicating a high rate of falls

with treadmill training.68

Several limitations should beacknowledged. It would have beenunethical to have a no-exercise con-trol group for a 16-month study,given the growing evidence thatexercise benefits people with PD.Cross-sectional data are availableacross stages of PD for the functionalmeasures used in this study59; how-ever, longitudinal data are lacking forthese measures. Such data will allowfurther interpretation of data in this

investigation.

Our study was conducted in Colo-rado, one of the fittest states in thecountry. These individuals may bemore likely to exercise than peoplein other areas of the country, evenif they are assigned to the controlgroup, possibly affecting applicabil-ity of our results to other populations.

With regard to outcomes, when thisstudy was initiated, there was noexpectation that exercise might ame-liorate the UPDRS motor subscalescores. Hence, we did not collectdata in the off-medication state.However, we did control forlevodopa equivalents, which shouldhave adjusted for any bias due tomedication effects. Other measuresmight provide better estimates ofbalance in people with PD than does

the FRT; evidence in this regardlikewise became available after thisstudy was initiated.69

With regard to the interventions, the3 groups received different degreesof individualized attention and groupexperience, which could have con-founded the findings. On the otherhand, the interventions studied areclinically relevant, which was the

motivation for implementing themas described.

Finally, we do not have meaningfuldata on participants adherence.

Although we used exercise diaries,accuracy was insufficient for mean-ingful interpretation. In future stud-

ies, we recommend regular use ofactivity monitors to quantitativelycharacterize overall activity (eg, 1

week a month).70,71

From a clinical perspective, the find-ings suggest that both FBF and AEprograms may be important for peo-

Figure 2.Walking economy at speeds from 0.8 mph to 4 mph. The control group participated ina home-based program of exercises recommended by the National Parkinson Founda-tion,18 the AE group participated in a standard aerobic endurance program, and the FBFgroup participated in a flexibility/balance/function program specifically designed forpeople with Parkinson disease (PD). Oxygen uptake (V O

2, in mL/min/kg) is presented

for each group at 4 time points (baseline, 4, 10, and 16 months), illustrating theimprovement (less oxygen required) for the AE group, but not for the other 2 groups.Walking speeds (increased by 0.5 mph for 4 speeds) are determined for each participant

by the maximum walking speed achieved during the graded exercise test.





15/18

ple with early- and mid-stage PD.Findings support using the FBF pro-gram with individuals early in PD toimprove overall function and the AEprogram to improve long-term aero-

bic endurance. A refresher FBF pro-gram could be implemented, shouldflexibility and function begin todecline. The necessary dose and tim-ing of such a combined interventionare yet to be established. Based onthe lack of meaningful decline of anymeasures over the 16-month study,it appears that the Fitness Countsprogram (control) also confers somebenefits, although to a lesser extentthan the supervised programs. Possi-bly participating in a study with

monthly sessions was sufficient forthese individuals. Qualitative reportsfrom graduates of the 16-monthstudy65 emphasize that people needongoing support to maintain regularexercise. We strongly recommendthat clinicians find ways to assistindividuals with PD to develop andmaintain long-term exercise habits,including appropriate exercise pro-grams as well as continuedre-evaluation and support.

Dr Schenkman, Dr Schwartz, and Dr Kohrtprovided concept/idea/research design. DrSchenkman, Dr Baron, Dr Schwartz, and DrKohrt provided writing. Dr Hall, Dr Schwartz,Ms Mettler, and Dr Kohrt provided datacollection. Dr Schenkman, Dr Baron, DrSchwartz, Ms Mettler, and Dr Kohrt pro-vided data analysis. Dr Schenkman and MsMettler provided project management. DrSchenkman provided fund procurement. DrSchwartz and Dr Kohrt provided facilities/equipment. Ms Mettler provided clericalsupport. Dr Hall provided consultation

(including review of manuscript before sub-mission). The authors gratefully acknowl-edge members of the research team whomade this study possible and the partici-pants with Parkinson disease, without whomthere would have been no study.

This study was approved by the InstitutionalReview Board of the University of Colorado.

This research was presented at the Com-bined Sections Meeting of the AmericanPhysical Therapy Association; February912, 2011; New Orleans, Louisiana.

Table

4.

EstimatedSlopeDifferencesBetweenGroupsa

Measure

AEGroupvs

ControlGroup

FBFGroupvsControlGroup

AEGroupvsF

BFGroup

AEandFBFGroupsvs

ControlGroup

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

Estimated

Difference

X(SE)

95

%

CI

P

Estimated

Difference

X(SE)

95%

CI

P

CS-PFPscore

Total

0.1(0.2)

0.3to0.5

.546

0.4(0.2)

0.0to0.8

.047

0.3(0.2)

0.7to0.1

.173

0.3(0.2)

0.1to0.6

.136

FRTscore

Forward

0.0(0.1)

0.1to0.1

.638

0.0(0.1)

0.1to0.1

.502

0.1(0.1)

0.0to0.2

.257

0.0(0.0)

0.1to0.1

.911

UPDRSscore

ADL

0.2(0.1)

0.4to0.0

.020

0.2(0.1)

0.4to0.0

.023

0.0(0.1)

0.2to0.2

.925

0.2(0.1)

0.3to0.1

.008

Motor

0.3(0.2)

0.6to0.1

.137

0.1(0.2)

0.4to0.3

.753

0.2(0.2)

0.6to0.1

.234

0.2(0.2)

0.5to0.1

.293

Total

0.5(0.2)

0.9to0.1

.021

0.3(0.2)

0.7to0.1

.192

0.2(0.2)

0.7to0.2

.290

0.4(0.2)

0.8to0.0

.036

PDQ-39score

Total

0.3(0.2)

0.7to0.1

.172

0.3(0.2)

0.7to0.1

.193

0.0(0.2)

0.4to0.4

.939

0.3(0.2)

0.7to0.1

.124

a

Thecontrolgroupparticipatedinahome-basedprogramofexercisesrecommendedby

theNationalParkinsonFoundation,1

8

theAEgroupparticipatedinastandardaerobicenduran

ceprogram,and

theFBFgroupparticipatedinaflexibility/b

alance/functionprogramspecificallydesignedforpeoplewithParkinsondisease(PD).UPDRS

UnitedParkinsonsDiseaseRatingScale,ADLactivitiesofdaily

living,CS-PFPContinuousScalePhysicalFunctionalPerformanceTest,FRTFunctionalReachTest,PDQ-3939-itemParkinsonsDiseaseQuestionnaire,SEstandarderror,95%CI95%confidence

interval.



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This work was supported by grants fromthe National Institutes of Health (R01HD043770-04, Colorado CTSI TL1RR025778, P30 DK048520, and NS052487)and the Parkinsons Disease Foundation.

ClinicalTrials.gov identifier: NCT01257945.

DOI: 10.2522/ptj.20110472

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doi: 10.2522/ptj.20110472Originally published online July 19, 2012

2012; 92:1395-1410.PHYS THER.KohrtRobert S. Schwartz, Pamela Mettler and Wendy M.

Margaret Schenkman, Deborah A. Hall, Anna E. Barn,Disease: A 16-Month Randomized Controlled TrialExercise for People in Early- or Mid-Stage Parkinson

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