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Research

JAMA Neurology | Original Investigation

Effects of Mindfulness Yoga vs Stretching and


Resistance Training Exercises on Anxiety and
Depression for People With Parkinson Disease A
Randomized Clinical Trial
Jojo Y. Y. Kwok, PhD, MPH, BN, RN; Jackie C. Y. Kwan, MSocSc, PDMH, BSW, RSW; M. Auyeung, MBChB;
Vincent C. T. Mok, MD, MBBS; Claire K. Y. Lau, MSc, BN, APN; K. C. Choi, BSc, PhD; Helen Y. L. Chan, PhD, BSN, RN
Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease

IMPORTANCE Clinical practice guidelines support exercise for patients with Parkinson disease
(PD), but to our knowledge, no randomized clinical trials have tested whether yoga is superior
to conventional physical exercises for stress and symptom management.

OBJECTIVE To compare the effects of a mindfulness yoga program vs stretching and resistance
training exercise (SRTE) on psychological distress, physical health, spiritual well-being, and
health-related quality of life (HRQOL) in patients with mild-to-moderate PD.

DESIGN, SETTING, AND PARTICIPANTS An assessor-masked, randomized clinical trial using the
intention-to-treat principle was conducted at 4 community rehabilitation centers in Hong
Kong between December 1, 2016, and May 31, 2017. A total of 187 adults (aged 18 years)
with a clinical diagnosis of idiopathic PD who were able to stand unaided and walk with or
without an assistive device were enrolled via convenience sampling. Eligible participants
were randomized 1:1 to mindfulness yoga or SRTE.

INTERVENTIONS Mindfulness yoga was delivered in 90-minute groups and SRTE were delivered
in 60-minute groups for 8 weeks.

MAIN OUTCOMES AND MEASURES Primary outcomes included anxiety and depressive symptoms
assessed using the Hospital Anxiety and Depression Scale. Secondary outcomes included
severity of motor symptoms (Movement Disorder Society Unified Parkinson’s Disease Rating
Scale [MDS-UPDRS], Part III motor score), mobility, spiritual well-being in terms of perceived
hardship and equanimity, and HRQOL. Assessments were done at baseline, 8 weeks (T1), and
20 weeks (T2).

RESULTS The 138 participants included 65 men (47.1%) with a mean (SD) age of 63.7 (8.7)
years and a mean (SD) MDS-UPDRS score of 33.3 (15.3). Generalized estimating equation
analyses revealed that the yoga group had significantly better improvement in outcomes
than the SRTE group, particularly for anxiety (time-by-group interaction, T1: β, −1.79 [95% CI,
−2.85 to −0.69; P = .001]; T2: β, −2.05 [95% CI, −3.02 to −1.08; P < .001]), depression (T1: β,
−2.75 [95% CI, −3.17 to −1.35; P < .001]); T2: β, −2.75 [95% CI, −3.71 to −1.79; P < .001]),
perceived hardship (T1: β, −0.92 [95% CI, −1.25 to −0.61; P < .001]; T2: β, −0.76 [95% CI,
−1.12 to −0.40; P < .001]), perceived equanimity (T1: β, 1.11 [95% CI, 0.79-1.42; P < .001]; T2:
β, 1.19 [95% CI, 0.82-1.56; P < .001]), and disease-specific HRQOL (T1: β, −7.77 [95% CI,
−11.61 to −4.38; P < .001]; T2: β, −7.99 [95% CI, −11.61 to −4.38; P < .001]).

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Yoga
vs
Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

P CONCLUSIONS AND RELEVANCE Among patients with mild-to-moderate PD, the mindfulness yoga Supplemental content
program was found to be as effective as SRTE in improving motor dysfunction and mobility,
with the additional benefits of a reduction in anxiety and depressive symptoms and

Author Affiliations: Author affiliations are


listed at the end of this article.
Corresponding Author: Jojo Y. Y.
Kwok, PhD, MPH, BN, RN, School of
an increase in spiritual well-being and HRQOL. Nursing, Li Ka Shing Faculty of
Medicine, The University of Hong
Kong, 4/F, William MW Mong Block,
21 Sassoon Rd, Pokfulam, Hong Kong Special
TRIAL REGISTRATION CentreforClinicalResearchandBiostatisticsidentifier:CUHK_CCRB00522 Administrative Region
(jojo.yykwok@gmail.com).
JAMA Neurol. doi:10.1001/jamaneurol.2019.0534
Published online April 8, 2019.

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Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease

Parkinson disease (PD) is the second most common chronic Key Points
neurodegenerative disease with heterogeneoussymptomatology.1
Question Is yoga—a mindfulness-based exercise intervention— a
AlthoughPDischaracterized by 4 motor symptoms (resting tremor, safe and favorable coping strategy compared with conventional
rigidity, bradykinesia, and postural instability), patients with PD stretching and resistance training exercise for management of
experience a stress and symptoms in people with mild-to-moderate Parkinson
varietyofnonmotorsymptoms,includingneuropsychiatricproblems, disease?
cognitive impairment, sleep disturbances, and Findings In this randomized clinical trial that included 138
autonomicdysfunction.Psychologicaldistress,including anxiety and patients with Parkinson disease, the mindfulness yoga program
depression (frequently co-occuring), is common in patients with PD, appeared to be a safe and favorable coping strategy for patients
with a prevalence of 40% to 50%,2 and is associated with care with Parkinson disease to address their physical and emotional
dependency, poor work and social function, fast physical and cognitive needs. Compared with conventional stretching and resistance
training exercise, mindfulness yoga showed additional benefits
decline, increased dementia risk, and high mortality.3-6 Recent evidence
on psychological distress, spiritual well-being, and health-related
identifies functional impairment and psychological distress as quality of life, with comparable benefits related to motor
significant associating factors of impaired health-related quality of life symptoms and mobility.
(HRQOL)inpatientswithPD,7,8withpsychologicaldistresscontributing
Meaning Mindfulness yoga appeared to be an effective and safe
most to the variance in HRQOL (42.4%; P < .01).2 Despite the high
treatment option for patients with mild-to-moderate Parkinson
prevalence and substantial negative consequences of psychological
disease for stress and symptom management; further
distress, this problem is poorly recognized and rarely addressed. investigation is warranted to establish its long-term effect and
Because there is a lack of optimal pharmacologic management options, compliance.
adopting a complementary, nonpharmacologic approach to manage
stress and symptoms in patients with PD is indispensable.7
Exerciseandphysicaltherapyhavebeenrecommendedas exercises (SRTE) on psychological distress (primary outcome), as well
essentialcomponentsinPDrehabilitation,complementaryto as physical health, spiritual well-being, and HRQOL (secondary
pharmacotherapyandfunctionalsurgery.8-10Arecentsystematic review of outcomes) in patients with mild-tomoderate PD. Compared with
the long-term effects of exercise and physical therapy for patients with patients receiving SRTE, we hypothesized that patients with PD
PD concluded that most stretching randomly assigned to receive the mindfulness yoga program would
andresistancetrainingprogramshadclinicallysignificantbenefitsonmobili show a greater improvement in psychological distress in terms of
ty,gait,andbalanceamongpatientswithPDfor the duration of exercise anxiety and depressive symptoms, physical health in terms of motor
implementation.11 For instance, symptoms and mobility, spiritual well-being in terms of perceived
stretchingcanreducetheshorteningofflexormusclesthatcontribute to the equanimity and hardship, and HRQOL.
abnormally flexed posture in PD,8 and
resistancetrainingcanincreasemusclestrengthandenhancegait
performance.12,13 Besidesphysicalexercise,mind-
bodyexerciseshavebeenreportedtobethemostcommoncomplementary Methods
strategies adopted by patients with PD to enhance their physical and Study Design
holistic well-being.14 This study was an assessor-masked, multicentered, randomized clinical
Mind-body exercises adopt an integrative body-mindspirit trial of PD that compared MY-PD with SRTE. The trial protocol has
approach to achieve physical and mental benefits through physical been published,18 and the original trial protocol is available in
exertion.15 A 2016 meta-analysis16 concluded that mind-body exercises, Supplement 1. The setting was outpatient clinics and community-based
including yoga, dance, and tai chi, had immediate moderate-to-large rehabilitation facilities. The institutional review board of each site
beneficial associations with motor symptoms, postural instability, and (Hong Kong East Cluster Research Ethics Committee and Joint Chinese
functional mobility among patients with mild-to-moderate PD. University of Hong Kong–New Territories East Cluster Clinical
However, besides physical parameters, studies examining such effects Research Ethics Committee) approved the protocol. All participants
on psychosocial outcomes and HRQOL among patients with PD are provided written informed consent, and all data were anonymous. This
lacking. Because psychosocial factors play an important role in stress trial followed the Consolidated Standards of Reporting Trials Extension
and associated physical and psychosocial disability,2,17 mind-body (CONSORT Extension) reporting guideline.
exercise, which emphasizes mindfulness during physical exertion, may
be superior to conventional physical exercise for stress and symptom Study Participants
management in patients with PD. A mindfulness yoga program— Participants with idiopathic PD were enrolled using convenience
Mindfulness Yoga for PD (MY-PD)—that integrates and emphasizes sampling from December 1, 2016, to May 30, 2017. Participants were
mindfulness training in yoga practice was tailored for patients with mild- recruited through 2 regional neurology outpatient clinics and 4 centers
to-moderate PD. of the Hong Kong Society of Rehabilitation, Hong Kong Parkinson’s
This randomized clinical trial examined the comparative effects of Disease Association. These sites cover the 3 main regions in Hong
MY-PD and stretching and resistance training Kong, including Hong Kong Island, Kowloon, and the New Territories.

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Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

Participants were eligible for inclusion in the trial if they had a clinical accordingtoamanualizedprotocolinwhichallinstructorswere trained. The
diagnosis of idiopathic PD with a disease severity rating of stage 1 on MY-PD was delivered by a yoga instructor with mindfulness-based
the Hoehn and Yahr scale 3 (rated on a scale of 1-5, with higher numbers stress reduction teacher qualifications, whereas SRTE was given by 2
indicating more severe disease), were older than 18 years, could stand qualified fitness instructors. All instructors were experienced in
unaided and walk with or without an assistive device, and could give teaching people with
written consent. Participants were excluded if they were currently chronicillnesses.Participantsineachinterventionweregiven an
receiving pharmacologic (eg, antidepressants) or surgical treatments information booklet covering instructions for home practice. An
(eg, deep brain stimulation) for psychiatric disorders (eg, schizophrenia, information booklet with instructions for each intervention was given
psychosis, or major depressive disorder), were currently participating in to all participants, whereas audios and
another behavioral or pharmacologic trial or instructorled exercise videosweregivenonlytotheparticipantsintheMY-PDgroup (eg, body
program, had significant cognitive impairment (Abbreviated Mental scan, meditation, yoga movements, and controlled
Test Score <6 [range, 0-10]),19 or had debilitating conditions other than breathing).Inaddition,sessionswereaudiotaped,andastudy
PD (eg, hearing or vision impairment) that could impede full investigator(J.Y.Y.K.)monitoredinstructors’adherencetothe protocol
participation in the study. using the audio recording for at least 2 sessions per group.

Screening, Baseline Testing, and Randomization Outcome Measures


Prescreening was done via telephone and in neurology clinics. Outcomeassessorsweretrainedandmaskedtogroupallocation. Each
Participants who met the criteria underwent baseline assessments. participant was invited to the nearby community
Participants were randomly allocated to experimental or control groups rehabilitationcentertoconductaface-to-faceclinicalassessment and
at a 1:1 ratio through a computerbased permuted block randomization interview. All assessments were conducted during
with a block size of 8. The randomization sequence was generated by an the“onstate”oflevodopatreatmenttominimizemotorfluctuations among
independent research coordinator, and the details of the group allocation participants, if indicated. All outcome measures were administered at
were concealed on cards placed inside sequentially numbered, sealed each time point: baseline (T0),
opaque envelopes. 8weeks(immediatelyaftertheintervention)(T1),and20weeks (3 months
after the intervention) (T2).
The primary outcome, psychological distress in terms of anxiety
Interventions
Mindfulness Yoga for PD and depressive symptoms, was measured using the validated Hospital
For 8 weeks, the intervention group received a weekly 90-minute session Anxiety and Depression Scale (HADS) (Chinese-Cantonese
of MY-PD (eMethods 1 in Supplement 2). In addition, all participants language),20,21 which is a self-report questionnaire that consists of
were encouraged to perform 20-minute home-based practice twice a anxiety and depression subscales. Each subscale consists of 7 items, and
week. The MY-PD protocol includes a progressive and stepwise each item is rated on a 4-point scale. A high score represents a high level
delivery of the 12 basic Hatha yoga poses: sun salutations (60 minutes) of psychological distress. The HADS has been suggested for use in the
with controlled breathing (15 minutes) and mindfulness meditation (15 population with PD because somatic symptoms that may potentially
minutes). The MY-PD protocol was developed and guided by the theory overlap parkinsonian manifestations are not assessed on this scale. 22,23
of self-transcendence (eMethods 2 in Supplement 2)16 and grounded on Also, HADS focuses on measuring the negative emotions of anxiety and
the findings obtained from a systematic review13 and a mixed-methods depression, which have been reported as being the most prominent
study of the illness experience and unmet care needs of local patients psychological factors in patients with PD. In the present study, the levels
with PD.2,17 of anxiety and depression were considered to be clinically relevant at a
cutoff value of at least 8 on each subscale (anxiety: sensitivity, 0.89;
specificity, 0.75; depression: sensitivity, 0.80; specificity, 0.88)24 and at
Stretching and Resistance Training Exercises
least 15 for the full scale (sensitivity, 0.79; specificity, 0.80).20 The
For 8 weeks, the control group received a weekly 60-minute session of
minimal clinical important difference of HADS anxiety scores was 1.32
SRTE (eTable 1 in Supplement 2). All participants were also
and of HADS depression scores was 1.40.25
encouraged to perform 20-minute home-based practice twice a week.
Secondaryoutcomesincluded(1)severityofmotorsymptoms as
The SRTE protocol consisted of a progressive set of warm-up, resistance
measured by the validated Movement Disorders Society Unified
training and stretching, and cool-down exercises, which were reviewed
Parkinson’s Disease Rating Scale (MDSUPDRS), Part III (Chinese
by 2 physiotherapists to confirm the validity for the patients with PD.
version),26 which covers domains related to tremor, rigidity,
The integration of an active control group was aimed at
bradykinesia, gait, and postural instability; (2) mobility as measured by
counteractingtheconfoundingeffectsofregularsocialinteraction among
the validated Timed
participants. The interventions were
UpandGoTest27,28;(3)spiritualwell-beingasmeasuredbythe
comparableinformat(group),frequency(weekly),duration(8weeks,
althoughthemindfulnessyogahadanadditional30minutes per session),
number of participants per group (15-20 participants per session), and
venue (activity rooms in community rehabilitation centers). Each
intervention was delivered
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Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease

emotional well-being, social support, cognitions, communication,


bodily discomfort, and stigma.
Adverse Events
Adverse events were identified during the intervention sessions and by
Excluded follow-up interview questions about significant
discomfort,pain,orharmcausedbytheintervention.Participants were
Severe mobility impairment
instructed to inform the research team if they encountered any adverse
Cognitive impairment event related to the study.

Sample Size
According to a meta-analysis of the association of yoga with
depressioncomparedwithaerobicexercises,32 amoderateeffect size of
0.59 was reported for people who presented with depressive symptoms.
Assuming an attrition rate of 25%,16 a sample size of 126 participants
with 63 participants per arm was required to provide a 2-arm trial with
80% power to detectaneffectsizeofatleast0.59ata5%levelofsignificance.

Statistical Analysis
Excluded Excluded Descriptive statistics were used to summarize the demographics, health
conditions, and clinical outcomes of the participants at each time point.
The normality of variables was assessed using the skewness statistic and
Reallocation to
normal probability plot. All participants were examined at T0, T1, and
T2 for changes in psychological distress, motor symptoms, mobility,
spiritual well-being, and HRQOL. The intention-totreat principle was
applied. Generalized estimating equation models, specifically with a
first-order autoregressive structure, were used to assess the differential
change in the primary outcome variable (HADS score) and secondary
outcome variables (MDS-UPDRS, Timed Up and Go Test, Holistic
Well-being Scale, and 8-item Parkinson’s Disease Questionnaire scores)
Family issues Disinterest between the 2 groups at T1 and T2 compared with T0 for both outcomes.
Family issue Completers and noncompleters were compared to check for any
differences in demographic characteristics and health conditions.
Statistical analysis was performed using SPSS statistical software,
Disinterest
version 22.0 (IBM Corporation). All statistical tests were 2-tailed with
a 5% level of statistical significance.

Disinterest Disinterest
Family issues Family issue Results
Of 187 potential participants screened, 31 did not meet eligibility criteria
and 18 declined to participate (enrollment rate: 73.8%) (Figure). Of the
138 participants randomized, 71 were in the experimental group and 67
were in the control group. ParticipantsrandomizedtotheMY-
Included in the analysis Included in the analysis
PDgroupattendedatleast 1 session, whereas 15 of 67 participants
(22.4%) randomized
totheSRTEgroupdidnotattendanysessions.Themean(SD) attendance
rates were 6.1 (1.9) sessions for the MY-PD group and 6.1 (2.4) sessions
validatedHolisticWell-beingScale(Chineseversion),29 which covers 2 for the SRTE group; 50 of 71 participants (70.4%) attended at least 6
major concepts of spiritual health (perceived hardship and perceived sessions of MY-PD, and 55 of 71 participants (77.6%) attended at least
equanimity [enduring happiness]) 6 sessions of SRTE. The overall dropout rates were 21 of 138 (15.2%)
(eMethods3inSupplement2);and(4)HRQOLasmeasuredby at T1 (MY-PD: 13 of 71 [18.3%]; SRTE: 8 of 67 [11.9%]) and 26 of
thevalidateddisease-specific8-itemParkinson’sDiseaseQuestionnaire 138 (18.8%)atT2(MY-PD:14of71[19.7%];SRTE:12of67[17.9%]). The
(Chinese version),30,31 which yields a summary index score capturing compliance rates of home practice during the
disease-specific HRQOL regarding mobility, activities of daily living, interventionperiodwere70.4%(50of71)fortheMY-PDand73.3%(49 of
67) for the SRTE groups.
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Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

Participants, No. (%)

Characteristic All (N = 138) Yoga (n = 71) Control (n = 67) P Valuea


Age, mean (SD), y 63.6 (8.7) 63.7 (8.2) 63.5 (9.3) .90

Sex

Male (47.1) (52.1) 28 (41.8)


.22
Female (52.9) (47.9) 39 (58.2)

Marital status

Single, separated, divorced, or widowed (21.7) (19.7) 16 (23.9)


.55
Married (78.3) (80.3) 51 (76.1)

No. of children, mean (SD) 1.7 (1.0) 1.7 (1.0) 1.7 (1.1) .82

Educational level

Illiterate or primary (18.1) (26.8) 6 (9)

Secondary (56.5) (52.1) 41 (61.2) .02


Tertiary (25.4) (21.1) 20 (29.9)

Living status

Alone (10.1) (16.9) 2 (3)


.01
With spouse, family, or friends (89.9) (83.1) 65 (97)

Social Security allowance (73.9) (76.1) 48 (71.6) .56

Hoehn and Yahr stageb

1 (1.4) 2 (3)

2 (30.4) (32.4) 19 (28.4) .32


3 (68.1) (67.6) 46 (68.7)

Levodopa equivalent dose, mean (SD) 2615.0 (7186.8) 2685.0 (7870.6) 2541.1 (6442.0) .91

Table 1. Baseline Sociodemographic Characteristics of the Participants


a 2
For categorical variables, a χ test was used, and for continuous variables, an independent t test was used when variables were compared between the 2 groups.
b Rated on a scale of 1 to 5, with higher numbers indicating more severe disease.
Baseline Characteristics of Participants completed the intervention vs those who did not complete the
Intervention and control groups were similar in intervention (eTable 2 in Supplement 2).
sociodemographicandclinicalcharacteristicsatbaselineexceptmorepartic
ipantsfromtheMY-PDgrouphadreceivedlesseducationand Coprimary Outcomes
livedalone(Table1).Themean(SD)ageofparticipantswas63.6 (8.7) years, Foranxietyanddepressivesymptoms,thegroupsdifferedsignificantly at
ranging from 38 to 85 years, and 73 of 138 were the T1 (P = .001) and T2 (P < .001) end points (Table 2). Compared
female(52.9%).MildPD(HoehnandYahrscale,stage1–2)was with the SRTE group, the MY-PD group demonstrated significantly
seenin44of138participants(31.9%),andmost(94;68.1%)had moderate better improvement in anxiety (time-by-
PD (Hoehn and Yahr scale, stage 3). The mean (SD) MDS- groupinteraction,T1:β,−1.79[95%CI,−2.85to−0.69; P = .001]; T2: β,
UPDRSscorewas33.3(15.3)amongallparticipants.Forpsychological −2.05 [95% CI, −3.02 to −1.08; P < .001]) and depressive symptoms
distress, 52 of 138 (37.7%) presented with clinically (T1: β, −2.75 [95% CI, −3.17 to −1.35; P <
significantanxietysymptomsand48of138(34.8%)withclinicallysignifica .001];T2:β,−2.75[95%CI,−3.71to−1.79;P < .001]).Inthe SRTE group,
ntdepressivesymptoms,withamean(SD)HADS score of 12.4 (6.7). No no significant improvement was noted in anxiety and depressive
significant heterogeneity of the symptoms across time points.
demographicdataandbaselinecharacteristicswasfoundamongthose who

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Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease

Secondary Outcomes
Both groups showed a significant reduction in motor
symptoms(mindfulnessyoga,T1:β,−13.90[95%CI,–15.85to–11.95, P <
.001]; T2: β, −11.59 [95% CI, −13.61 to −9.56; P < .001]); SRTE, T1:
β, −8.71 [95% CI, −10.94 to −6.48; P < .001]; T2: β,
−6.88[95%CI,−9.08to−4.68;P < .001]).Comparedwiththe SRTE group,
the MY-PD group showed significant improvementinMDS-
UPDRSmotorscores(T1:β,−5.19[95%CI,−8.15 to −2.24; P = .001]; T2:
β, −4.71 [95% CI, −7.70 to −1.72; P = .002]), spiritual well-being in
terms of perceived hardship(time-by-
groupinteraction,T1:β,−0.92[95%CI,−1.25to −0.61;P <
.001];T2:β,−0.76[95%CI,−1.12to−0.40;P < .001]) and perceived
equanimity (T1: β, 1.11 [95% CI, 0.79-1.42; P <
.001];T2:β,1.19[95%CI,0.82-1.56;P <
.001]),anddiseasespecificHRQOL(T1:β,−7.77[95%CI,−11.61to−4.38;P
< .001]; T2: β, −7.99 [95% CI, −11.61 to −4.38; P < .001]) at T1 and
T2, whereas no significant between-group difference was noted in the
Timed Up and Go Test scores at either end point.

Adverse Events
Threeparticipants(4.2%)fromtheMY-PDgroupreportedtemporary mild
knee pain associated with yoga, which resolved with the use of a prop
(placing a thick towel on the knee); no medical attention was needed.
Two participants (3.0%) from the SRTE group reported temporary mild
knee pain when squatting or after squatting but required no medical
attention. No serious adverse events were reported.

Discussion
ResultsindicatethatMY-PDwassuperiortoconventionalSRTE
formanaginganxietyanddepressivesymptomsatT1andT2.
Theimprovementofanxietyanddepressivesymptomsinthe MY-PD group
was considered to be statistically and clinically significant. Although the
participants in the MY-PD group

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Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

Table 2. Generalized Estimating Equation Analysis for the Comparison of Outcomesa


Mean (SD) Group Effectb Time Effectc Group × Time Effectd

β (95% CI) P Value


Outcome Experimental Control β (95% CI) P Value β (95% CI) P Value
HADS-anxiety

T0 6.32 (3.57) 5.66 (3.96) NA NA NA NA


0.67 −1.79 (−2.85 to −0.69) .001e
T1 3.97 (3.57) 5.22 (3.84) .30 −0.46 (−1.22 to 0.30) .23
(−0.58 to 1.92)
T2 3.04 (3.06) 4.95 (3.49) −0.72 (−1.43 to −0.01) .05 −2.05 (−3.02 to −1.08) <.001
HADS-depression

T0 6.69 (3.36) 6.16 (3.64) NA NA NA NA


0.53 −2.75 (−3.17 to −1.35) <.001
T1 4.10 (3.18) 5.90 (3.65) .38 −0.32 (−1.00 to 0.37) .36
(−0.64 to 1.69)
T2 3.53 (2.84) 6.00 (3.71) −0.20 (−0.94 to 0.54) .60 −2.75 (−3.71 to −1.79) <.001
MDS- UPDRS III

T0 34.90 (14.88) 31.64 (15.59) NA NA NA NA


3.22 −5.19 (−8.15 to −2.24) .001e
T1 21.10 (13.61) 22.53 (14.66) .21 −8.71 (−10.94 to −6.48) <.001
(−1.84 to 8.27)
T2 22.41 (11.31) 23.25 (12.84) −6.88 (−9.08 to −4.68) <.001 −4.71 (−7.70 to −1.72) .002e
TUGe

T0 17.54 (15.95) 14.05 (6.04) NA NA NA NA


0.06 −0.01 (−0.08 to 0.05) .72
T1 14.72 (14.77) 12.41 (5.04) .28 −0.11 (−0.17 to −0.06) <.001
(−0.05 to 0.18)
T2 12.36 (6.42) 13.47 (16.43) −0.16 (−0.21 to −0.11) <.001 0.00 (−0.08 to 0.08) .99
HWS-perceived
hardshipf
T0 4.04 (1.54) 3.88 (1.70) NA NA NA NA
0.17 −0.92 (−1.25 to −0.61) <.001
T1 3.22 (1.39) 4.02 (1.53) .55 0.14 (−0.08 to 0.36) .22
(−0.37 to 0.70)
T2 3.12 (1.55) 3.89 (1.73) 0.01 (−0.27 to 0.29) .94 −0.76 (−1.12 to −0.40) <.001
HWS-perceived
equanimityg
T0 6.47 (1.38) 6.82 (1.21) NA NA NA NA
−0.34 1.11 (0.79 to 1.42) <.001
T1 7.58 (1.19) 6.78 (1.19) .12 −0.03 (−0.27 to 0.21) .83
(−0.77 to 0.09)
T2 7.60 (1.41) 6.57 (1.61) −0.20 (−0.48 to 0.09) .18 1.19 (0.82 to 1.56) <.001
PDQ-8 summary
index
T0 9.79 (5.02) 9.21 (5.26) NA NA NA NA
1.81 −7.77 (−11.61 to −4.38) <.001
T1 7.57 (4.68) 9.66 (5.05) .51 0.38 (−2.60 to 3.35) .80
(−3.51 to 7.14)
T2 6.04 (4.76) 8.78 (5.51) −1.63 (−4.32 to 1.06) .24 −7.99 (−11.61 to −4.38) <.001
Abbreviations: HADS, Hospital Anxiety and Depression Scale; HWS, Holistic The control group (group = 1) and the baseline measurement (time = 0) were
Well-being Scale; MDS-UPDRS III, Movement Disorders Society United the reference categories in the generalized estimating equation model and its
Parkinson’s Disease Rating Scale, Part III; NA, not applicable; PDQ-8, 8-item corresponding null variables. b Group effect was defined as group differences at
Parkinson’s Disease Questionnaire; TUG, Timed Up and Go Test; T0, baseline; baseline between intervention and control groups.
c
T1, immediately after intervention (8 weeks); T2, 3 months after intervention
Time effect at T1 defined as change of scores for control group at T1
(20 weeks).
a
compared with T0; T2 defined as change of scores for control group at T2
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Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease

compared with T0. d Group × time effect at T1 defined as additional change of e With log transformation in the generalized estimating equation
scores for intervention group compared with control group at T1; T2 defined model.
f
as additional change of scores for intervention group compared with control
group at T2. HWS-perceived hardship defined as emotional vulnerability, bodily
irritability, and spiritual disorientation. g HWS-perceived equanimity defined as
nonattachment, mindful awareness, general vitality, and spiritual self-care.
reported significantly greater improvement in MDS-UPDRS These findings are consistent with the conclusions of various recent
scorescomparedwiththoseintheSRTEgroupduringthestudy systematic reviews38,39 that reported that mindfulness-based
period,thedifferencesinthemeanscoresbetweenthe2groups interventions had beneficial associations with the physical and mental
wereconsideredtobeclinicallyinsignificant.Thus,MY-PDwas health of patients with chronic conditions. Through the practice of
aseffectiveasSRTEinimprovingmotordysfunctionandmobility, with mindfulness, patients learn to relate differently to their physical
additional benefits related to perceived hardship, perceived equanimity, symptoms with a nonjudgmental attitude, such that when new symptoms
and HRQOL in people with PD. emerge, the consequences are less significantly disturbing. 40,41 In
TheMY- addition to preserving physical and functional capacities, the
PDgrouphadgreaterimprovementinpsychospiritualoutcomes,includinga mindfulness yoga program appeared to be a favorable strategy for stress
nxietyanddepressivesymptoms,perceived hardship, perceived and symptom management among patients with PD.
equanimity, and HRQOL at T1 and Our findings of the increased effects of mindfulness yoga
T2comparedwiththeSRTEgroup.Effectsofmindfulnessyoga in atT1toT2follow-upregardingpsychospiritualoutcomescontrasted with
improving psychological outcomes were moderate to large, which has the findings of other studies of dance therapy42 and Qigong43,44
been typical of evidence-based treatments conducted in the same population. In those
recommendedforpsychiatricconditionsofPD.33Thesebenefitswere studies,thetreatmenteffectsdecreasedatfollow-up.Thissuggests that
remarkable because the participants who received the MY-PD mindfulness-based interventions may provide patients with long-lasting
intervention attended a mean of only 6 sessions. skills effective for stress and symptom management. Substantial residual
Both groups showed significant improvement in physical outcomes gains of mindfulness practices have been reported for psychiatric
related to motor symptoms and mobility, with no statistically and treatments. Shapiro and Carlson45 highlighted the dynamic and evolving
clinically significant superiority noted. These findings were consistent natureofmindfulnessskills,whichwouldcontinuetogrowand deepen
with the conclusion of a 2017 systematic review11 that reported exercise alongside practice. Morgan46 found that the residual gains of
interventions had beneficial effects on the physical health of patients mindfulness skills were significantly associated with reductions in
with PD. anxiety and worry and with improved HRQOL. The present-focused
This study also partially confirmed the findings of another review of nature of mindfulness practice may exertalong-
exercise interventions in PD34 that found that physical exercise lastingbeneficialeffectasanemotionalcopingskill tocounterthefuture-
interventions had a positive impact on physical and functional orientednatureofanxietyandworryand the past-oriented nature of
capacities, but there was inconsistent evidence of its effects on nonmotor depression and rumination.
symptoms and the psychosocial aspects of life. Integrating mindfulness Althoughtheresidualgainsofmindfulnessskillswerenotmeasured in the
training into evidence-based exercise prescription, such as stretching present study, the results highlight the importance of continual
and progressive resistance exercises,35,36 could be considered in future mindfulness practice in daily living.
PD rehabilitation to optimize patients’ well-being. To complement the subjective self-reported outcomes regarding
Our study findings showed that only the MY-PD group psychological distress in the present study, future research should
demonstrated significant improvement regarding the psychospiritual integrate the use of objective
aspects of life. Mindfulness yoga has been shown to be more effective psychoneuroimmunologicmarkers(suchascortisolandcytokines)toelucid
than conventional physical exercises for psychological distress ate the mediating effects of mindfulness yoga on stress and
management. The noticeable success of the mindfulness yoga program inflammatory responses in relation to progression of PD. Research to
in improving psychospiritual well-being confirms the mindfulness evaluate the long-term benefits and compliance of mindfulness yoga,
component of the interventions. identify the reasons for
Mindfulness,amodernBuddhistmeditationpractice,emphasizesthen noncompliance,determinetheminimumdoserequired,andperformcosteff
onjudgmentalacceptanceofpeopleandsymptoms and the value of being ectiveness analysis is also necessary.
in the here and now.37 From the Buddhist context, hardship is inherent Compared with other relatively well-established mindfulness
in life processes, practices, including 8-week mindfulness-based stress reduction and
whereasnonattachmenttopleasuresandhardshipbringsabout emotional cognitive behavioral therapy, our mindfulness yoga program adopts a
stability. Although the current study is not dynamic exercise approach of mindfulness practice that relies on
intendedtoemphasizeBuddhistphilosophyorreligion,thepatients with PD physical exertion to achieve physiopsychospiritual benefits. Further
who engaged in mindfulness practice research is needed to compare different approaches of mindfulness
inevitablyexhibitedincreasedspiritualself-care.Thus,theymayhave practices, for example, exercise-oriented yoga vs meditation-oriented
cultivated a greater acceptance toward hardship and perceived less mindfulness. Regarding the cultural popularity of various mindfulness
hardship and more equanimity while confronting the vulnerable practices, a better understanding of the different mindfulness practices
conditions of PD. is crucial to enable patients and health care professionals to select the

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Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

best practice to optimize the benefits, satisfaction, adherence, and toenhanceparticipants’interest,uptake,andadherenceofthe control
sustainability for each patient. intervention. We purposely excluded people with
severePDwhohadseveremotorlimitations,andtheattritionrates
Strengths and Limitations of15.2%atT1and18.8%atT2shouldbeacknowledged.Theresults were
Studystrengthsincludeanassessor- based on a unique population of people with mildto-
masked,randomizedclinicaldesignwithlargesampleandadequatestatistic moderatePDwhoattendedthefollow–upsessions.Allthese
alpowerto detectaclinicallymeaningfuleffect,multiplefollow-uptime factorsmaylimitthegeneralizabilityofthestudyfindingstothe entire PD
points to elucidate the residual effects of interventions, involvement of population.
an active control group, and comprehensive measurement of Conclusions
physiopsychospiritual outcomes.
Among people with mild-to-moderate PD, mindfulness yoga
The limitations of this study must be acknowledged.
comparedwithconventionalSRTEresultedingreaterimprovement in
Expectationbiasmayexistbecauseparticipantswereawareof
psychospiritual and HRQOL outcomes and had similar benefits on
thetreatmentallocation.Selectionbiasmayarisebecausestudy
physical outcomes, including motor symptoms and mobility. These
participantswereenrolledthroughconveniencesampling.The
volunteersamplemightbemoreactiveinreachingouttocommunityresource findings suggest that mindfulness yoga is an effective treatment option
sandmorewillingtoexercisecomparedwith those who refused to for patients with PD to
participate or withdrew from the study. There might be potential bias managestressandsymptoms.ConsideringthatPDisnotonly a physically
based on female predominance andearlydropout(n = limiting condition but also a psychologically distressing life event,
15)intheSRTEgroup.Femalesweremore interested in receiving health care professionals should adopt
mindfulness yoga intervention. Because SRTE was more commonly aholisticapproachinPDrehabilitation.Futurerehabilitation programs
prescribed for PD could consider integrating mindfulness skills into physical therapy to
rehabilitation,futurecontrolmayincorporatemoreinnovativedesigns, enhance the holistic well-being of people with neurodegenerative
suchasperformingresistancetrainingonanunstabledevice,12 conditions.
ARTICLE INFORMATION Accepted for Statistical analysis: Kwok, Choi. Association, the Association of Hong Kong Nursing
Publication: January 11, 2019. Obtained funding: Kwok. Staff, and the Y. K. Pao Foundation Centre for
Administrative, technical, or material support: Nursing Excellence in Chronic Illness Care provided
Published Online: April 8, 2019. Kwok, Kwan, Auyeung, Mok, Lau. support to promote the mindfulness yoga program
doi:10.1001/jamaneurol.2019.0534 Supervision: Kwok, Mok, Chan. for chronic illness management in the community.
Author Affiliations: School of Nursing, Li Ka Shing We thank the study participants.
Conflict of Interest Disclosures: None reported.
Faculty of Medicine, The University of Hong Kong,
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