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

Supplemental content

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) Author Affiliations: Author affiliations are
years and a mean (SD) MDS-UPDRS score of 33.3 (15.3). Generalized estimating equation listed at the end of this article.

analyses revealed that the yoga group had significantly better improvement in outcomes Corresponding Author: Jojo Y. Y.
Kwok, PhD, MPH, BN, RN, School of
than the SRTE group, particularly for anxiety (time-by-group interaction, T1: β, −1.79 [95% CI,
Nursing, Li Ka Shing Faculty of
−2.85 to −0.69; P = .001]; T2: β, −2.05 [95% CI, −3.02 to −1.08; P < .001]), depression (T1: β, Medicine, The University of Hong
−2.75 [95% CI, −3.17 to −1.35; P < .001]); T2: β, −2.75 [95% CI, −3.71 to −1.79; P < .001]), Kong, 4/F, William MW Mong Block,
21 Sassoon Rd, Pokfulam, Hong Kong Special
perceived hardship (T1: β, −0.92 [95% CI, −1.25 to −0.61; P < .001]; T2: β, −0.76 [95% CI,
Administrative Region
−1.12 to −0.40; P < .001]), perceived equanimity (T1: β, 1.11 [95% CI, 0.79-1.42; P < .001]; T2: (jojo.yykwok@gmail.com).
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]).

P
(Reprinted) 755
arkinson disease (PD) is the second
CONCLUSIONS AND RELEVANCE Among patients with mild-to-moderate PD, the mindfulness yoga most common chronic
program was found to be as effective as SRTE in improving motor dysfunction and mobility, neurodegenerative disease with
with the additional benefits of a reduction in anxiety and depressive symptoms and an heterogeneoussymptomatology.1
increase in spiritual well-being and HRQOL. AlthoughPDischaracterized by 4 motor
symptoms (resting tremor, rigidity,
TRIAL REGISTRATION CentreforClinicalResearchandBiostatisticsidentifier:CUHK_CCRB00522 bradykinesia, and postural instability),
patients with PD experience a

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 Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease
varietyofnonmotorsymptoms,includingneuropsychiatricproblems,
cognitive impairment, sleep disturbances, and
autonomicdysfunction.Psychologicaldistress,includinganxiety and
depression (frequently co-occuring), is common in patients with PD, with a
prevalence of 40% to 50%,2 and is associated with care dependency, poor
work and social function, fast physical and cognitive decline, increased
dementia risk, and high mortality. 3-6 Recent evidence identifies functional
impairment and psychological distress as significant associating factors of
impaired health-related quality of life
(HRQOL)inpatientswithPD,7,8withpsychologicaldistresscontributing most
to the variance in HRQOL (42.4%; P < .01).2 Despite the high prevalence
and substantial negative consequences of psychological distress, this
problem is poorly recognized and rarely addressed. Because there is a lack
of optimal pharmacologic management options, adopting a
complementary, nonpharmacologic approach to manage stress and
symptoms in patients with PD is indispensable.7
Exerciseandphysicaltherapyhavebeenrecommendedas
essentialcomponentsinPDrehabilitation,complementaryto
pharmacotherapyandfunctionalsurgery.8-10Arecentsystematic review of the
long-term effects of exercise and physical therapy for patients with PD
concluded that most stretching
andresistancetrainingprogramshadclinicallysignificantbenefitsonmobility,g
ait,andbalanceamongpatientswithPDfor the duration of exercise
implementation.11 For instance,
stretchingcanreducetheshorteningofflexormusclesthatcontribute to the
abnormally flexed posture in PD,8 and
resistancetrainingcanincreasemusclestrengthandenhancegait
performance.12,13 Besidesphysicalexercise,mind-
bodyexerciseshavebeenreportedtobethemostcommoncomplementary
strategies adopted by patients with PD to enhance their physical and
holistic well-being.14
Mind-body exercises adopt an integrative body-mindspirit approach to
achieve physical and mental benefits through physical exertion. 15 A 2016
meta-analysis16 concluded that mind-body exercises, including yoga, dance,
and tai chi, had immediate moderate-to-large beneficial associations with
motor symptoms, postural instability, and functional mobility among
patients with mild-to-moderate PD. However, besides physical parameters,
studies examining such effects on psychosocial outcomes and HRQOL
among patients with PD are lacking. Because psychosocial factors play an
important role in stress and associated physical and psychosocial
disability,2,17 mind-body exercise, which emphasizes mindfulness during
physical exertion, may be superior to conventional physical exercise for
stress and symptom management in patients with PD. A mindfulness yoga
program—Mindfulness Yoga for PD (MY-PD)—that integrates and
emphasizes mindfulness training in yoga practice was tailored for patients
with mild-to-moderate PD.
This randomized clinical trial examined the comparative effects of
MY-PD and stretching and resistance training
Key Points
Question Is yoga—a mindfulness-based exercise intervention— a safe
and favorable coping strategy compared with conventional stretching
and resistance training exercise for management of stress and
symptoms in people with mild-to-moderate Parkinson disease?
Findings In this randomized clinical trial that included 138 patients
with Parkinson disease, the mindfulness yoga program appeared to
be a safe and favorable coping strategy for patients with Parkinson
disease to address their physical and emotional needs. Compared
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Original Investigation Research
with conventional stretching and resistance training exercise,
mindfulness yoga showed additional benefits on psychological
distress, spiritual well-being, and health-related quality of life, with
comparable benefits related to motor symptoms and mobility.
Meaning Mindfulness yoga appeared to be an effective and safe
treatment option for patients with mild-to-moderate Parkinson
disease for stress and symptom management; further investigation is
warranted to establish its long-term effect and compliance.
exercises (SRTE) on psychological distress (primary outcome), as well as
physical health, spiritual well-being, and HRQOL (secondary outcomes) in
patients with mild-tomoderate PD. Compared with patients receiving
SRTE, we hypothesized that patients with PD randomly assigned to receive
the mindfulness yoga program would show a greater improvement in
psychological distress in terms of anxiety and depressive symptoms,
physical health in terms of motor symptoms and mobility, spiritual well-
being in terms of perceived equanimity and hardship, and HRQOL.
Methods
Study Design
This study was an assessor-masked, multicentered, randomized clinical
trial of PD that compared MY-PD with SRTE. The trial protocol has been
published,18 and the original trial protocol is available in Supplement 1. The
setting was outpatient clinics and community-based rehabilitation facilities.
The institutional review board of each site (Hong Kong East Cluster
Research Ethics Committee and Joint Chinese University of Hong Kong–
New Territories East Cluster Clinical Research Ethics Committee)
approved the protocol. All participants provided written informed consent,
and all data were anonymous. This trial followed the Consolidated
Standards of Reporting Trials Extension (CONSORT Extension) reporting
guideline.
Study Participants
Participants with idiopathic PD were enrolled using convenience sampling
from December 1, 2016, to May 30, 2017. Participants were recruited
through 2 regional neurology outpatient clinics and 4 centers of the Hong
Kong Society of Rehabilitation, Hong Kong Parkinson’s Disease
Association. These sites cover the 3 main regions in Hong Kong, including
Hong Kong Island, Kowloon, and the New Territories.
Participants were eligible for inclusion in the trial if they had a clinical
diagnosis of idiopathic PD with a disease severity rating of stage 1 on the
Hoehn and Yahr scale 3 (rated on a scale of 1-5, with higher numbers
indicating more severe disease), were older than 18 years, could stand
unaided and walk with or without an assistive device, and could give
written consent. Participants were excluded if they were currently
receiving pharmacologic (eg, antidepressants) or surgical treatments (eg,
deep brain stimulation) for psychiatric disorders (eg, schizophrenia,
psychosis, or major depressive disorder), were currently participating in
another behavioral or pharmacologic trial or instructorled exercise
program, had significant cognitive impairment (Abbreviated Mental Test
Score <6 [range, 0-10]),19 or had debilitating conditions other than PD (eg,
hearing or vision impairment) that could impede full participation in the
study.
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 Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease
Screening, Baseline Testing, and Randomization Prescreening was time point: baseline (T0), 8weeks(immediatelyaftertheintervention)
done via telephone and in neurology clinics. Participants who met the (T1),and20weeks (3 months after the intervention) (T2).
criteria underwent baseline assessments. Participants were randomly The primary outcome, psychological distress in terms of anxiety and
allocated to experimental or control groups at a 1:1 ratio through a depressive symptoms, was measured using the validated Hospital Anxiety
computer-based permuted block randomization with a block size of 8. The and Depression Scale (HADS) (Chinese-Cantonese language),20,21 which is
randomization sequence was generated by an independent research a self-report questionnaire that consists of anxiety and depression
coordinator, and the details of the group allocation were concealed on subscales. Each subscale consists of 7 items, and each item is rated on a 4-
cards placed inside sequentially numbered, sealed opaque envelopes. point scale. A high score represents a high level of psychological distress.
The HADS has been suggested for use in the population with PD because
Interventions somatic symptoms that may potentially overlap parkinsonian
Mindfulness Yoga for PD manifestations are not assessed on this scale. 22,23 Also, HADS focuses on
For 8 weeks, the intervention group received a weekly 90-minute session measuring the negative emotions of anxiety and depression, which have
of MY-PD (eMethods 1 in Supplement 2). In addition, all participants were been reported as being the most prominent psychological factors in patients
encouraged to perform 20-minute home-based practice twice a week. The with PD. In the present study, the levels of anxiety and depression were
MY-PD protocol includes a progressive and stepwise delivery of the 12 considered to be clinically relevant at a cutoff value of at least 8 on each
basic Hatha yoga poses: sun salutations (60 minutes) with controlled subscale (anxiety: sensitivity, 0.89; specificity, 0.75; depression:
breathing (15 minutes) and mindfulness meditation (15 minutes). The MY- sensitivity, 0.80; specificity, 0.88) 24 and at least 15 for the full scale
PD protocol was developed and guided by the theory of self-transcendence (sensitivity, 0.79; specificity, 0.80).20 The minimal clinical important
(eMethods 2 in Supplement 2)16 and grounded on the findings obtained difference of HADS anxiety scores was 1.32 and of HADS depression
from a systematic review13 and a mixed-methods study of the illness scores was 1.40.25
experience and unmet care needs of local patients with PD.2,17 Secondaryoutcomesincluded(1)severityofmotorsymptoms as measured
by the validated Movement Disorders Society Unified Parkinson’s Disease
Rating Scale (MDSUPDRS), Part III (Chinese version), 26 which covers
Stretching and Resistance Training Exercises
domains related to tremor, rigidity, bradykinesia, gait, and postural
For 8 weeks, the control group received a weekly 60-minute session of
instability; (2) mobility as measured by the validated Timed
SRTE (eTable 1 in Supplement 2). All participants were also encouraged
UpandGoTest27,28;(3)spiritualwell-beingasmeasuredbythe
to perform 20-minute home-based practice twice a week. The SRTE
protocol consisted of a progressive set of warm-up, resistance training and
stretching, and cool-down exercises, which were reviewed by 2
physiotherapists to confirm the validity for the patients with PD.
The integration of an active control group was aimed at
counteractingtheconfoundingeffectsofregularsocialinteraction among
participants. The interventions were
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
accordingtoamanualizedprotocolinwhichallinstructorswere trained. The
MY-PD was delivered by a yoga instructor with mindfulness-based stress
reduction teacher qualifications, whereas SRTE was given by 2 qualified
fitness instructors. All instructors were experienced in teaching people with
chronicillnesses.Participantsineachinterventionweregiven an information
booklet covering instructions for home practice. An information booklet
with instructions for each intervention was given to all participants,
whereas audios and videosweregivenonlytotheparticipantsintheMY-
PDgroup (eg, body scan, meditation, yoga movements, and controlled
breathing).Inaddition,sessionswereaudiotaped,andastudy
investigator(J.Y.Y.K.)monitoredinstructors’adherencetothe protocol using
the audio recording for at least 2 sessions per group.

Outcome Measures
Outcomeassessorsweretrainedandmaskedtogroupallocation. Each
participant was invited to the nearby community
rehabilitationcentertoconductaface-to-faceclinicalassessment and
interview. All assessments were conducted during
the“onstate”oflevodopatreatmenttominimizemotorfluctuations among
participants, if indicated. All outcome measures were administered at each
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 Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research

Figure. Flow Diagram Adverse Events

187 Patients assessed for eligibility
49 Excluded
31 Did not meet eligibility criteria
18 Receiving psychiatric drug
9 Severe mobility impairment
1 Cognitive impairment
1 Other central nervous
system disease
1 Major surgery within 1 mo
1 Secondary parkinsonism
18 Declined to participate
9 Interested but schedule conflict
9 Lack of interest
138 Randomized
Adverse events were identified during the intervention sessions and by
follow-up interview questions about significant
discomfort,pain,orharmcausedbytheintervention.Participants were
instructed to inform the research team if they encountered any adverse
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.

71 Randomized to intervention
70 Received intervention
14 Excluded
7 Discontinued intervention
2 Health conditions
2 Lack of motivation
1 Reallocation to
nursing home
1 Family problem
1 Out of town
1 Did not receive allocated
intervention because
of lack of motivation
58 Completed T1 follow-up
assessment
13 Lost to follow-up
4 Out of town
3 Family issues
2 Health conditions
1 Transportation issue
1 Reallocation to nursing home
1 Loss of contact
1 Disinterest
67 Randomized to control
62 Received intervention
16 Excluded
8 Discontinued intervention
5 Health conditions
3 Lack of motivation
5 Did not receive allocated
intervention
3 Health problems
2 Lack of motivation
59 Completed T1 follow-up
assessment
8 Lost to follow-up
4 Health conditions
2 Disinterest
1 Family issue
1 Schedule conflict
Statistical Analysis
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
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) between the 2 groups at T1
and T2 compared with T0 for both outcomes. Completers and
noncompleters were compared to check for any differences in demographic
characteristics and health conditions. Statistical analysis was performed
using SPSS statistical software, version 22.0 (IBM Corporation). All
statistical tests were 2-tailed with a 5% level of statistical significance.

57 Completed T2 follow-up 55 Completed T2 follow-up Results

assessment assessment
14 Lost to follow-up 12 Lost to follow-up Of 187 potential participants screened, 31 did not meet eligibility criteria
5 Health conditions 4 Health conditions and 18 declined to participate (enrollment rate: 73.8%) (Figure). Of the 138
3 Disinterest 3 Disinterest
1 Family issues 1 Family issue participants randomized, 71 were in the experimental group and 67 were in
1 Transportation issue 3 Schedule conflict the control group. ParticipantsrandomizedtotheMY-
1 Reallocation to nursing home 1 Out of town
1 Loss of contact PDgroupattendedatleast 1 session, whereas 15 of 67 participants (22.4%)
2 Schedule conflict randomized totheSRTEgroupdidnotattendanysessions.Themean(SD)
attendance rates were 6.1 (1.9) sessions for the MY-PD group and 6.1 (2.4)
71 Included in the analysis 67 Included in the analysis sessions for the SRTE group; 50 of 71 participants (70.4%) attended at
least 6 sessions of MY-PD, and 55 of 71 participants (77.6%) attended at
least 6 sessions of SRTE. The overall dropout rates were 21 of 138 (15.2%)
at T1 (MY-PD: 13 of 71 [18.3%]; SRTE: 8 of 67 [11.9%]) and 26 of 138
(18.8%)atT2(MY-PD:14of71[19.7%];SRTE:12of67[17.9%]). The
validatedHolisticWell-beingScale(Chineseversion),29 which covers 2 major
compliance rates of home practice during the
concepts of spiritual health (perceived hardship and perceived equanimity
interventionperiodwere70.4%(50of71)fortheMY-PDand73.3%(49 of 67)
[enduring happiness])
for the SRTE groups.
(eMethods3inSupplement2);and(4)HRQOLasmeasuredby
thevalidateddisease-specific8-itemParkinson’sDiseaseQuestionnaire
(Chinese version),30,31 which yields a summary index score capturing
disease-specific HRQOL regarding mobility, activities of daily living,
emotional well-being, social support, cognitions, communication, bodily
discomfort, and stigma.

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

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 Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease Original Investigation Research
Baseline Characteristics of Participants Discussion
Intervention and control groups were similar in
ResultsindicatethatMY-PDwassuperiortoconventionalSRTE
sociodemographicandclinicalcharacteristicsatbaselineexceptmoreparticipan
formanaginganxietyanddepressivesymptomsatT1andT2.
tsfromtheMY-PDgrouphadreceivedlesseducationand
Theimprovementofanxietyanddepressivesymptomsinthe MY-PD group
livedalone(Table1).Themean(SD)ageofparticipantswas63.6 (8.7) years,
was considered to be statistically and clinically significant. Although the
ranging from 38 to 85 years, and 73 of 138 were
participants in the MY-PD group
female(52.9%).MildPD(HoehnandYahrscale,stage1–2)was
seenin44of138participants(31.9%),andmost(94;68.1%)had moderate PD
(Hoehn and Yahr scale, stage 3). The mean (SD) MDS-
UPDRSscorewas33.3(15.3)amongallparticipants.Forpsychological distress,
52 of 138 (37.7%) presented with clinically
significantanxietysymptomsand48of138(34.8%)withclinicallysignificantde
pressivesymptoms,withamean(SD)HADS score of 12.4 (6.7). No
significant heterogeneity of the
demographicdataandbaselinecharacteristicswasfoundamongthose who
completed the intervention vs those who did not complete the intervention
(eTable 2 in Supplement 2).

Coprimary Outcomes
Foranxietyanddepressivesymptoms,thegroupsdifferedsignificantly at the T1
(P = .001) and T2 (P < .001) end points (Table 2). Compared with the
SRTE group, the MY-PD group demonstrated significantly better
improvement in anxiety (time-by-groupinteraction,T1:β,−1.79[95%CI,
−2.85to−0.69; P = .001]; T2: β, −2.05 [95% CI, −3.02 to −1.08; P < .001])
and depressive symptoms (T1: β, −2.75 [95% CI, −3.17 to −1.35; P
< .001];T2:β,−2.75[95%CI,−3.71to−1.79;P < .001]).Inthe SRTE group, no
significant improvement was noted in anxiety and depressive symptoms
across time points.

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.

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

Table 2. Generalized Estimating Equation Analysis for the Comparison of Outcomes a

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
e
TUG

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 Well-
being Scale; MDS-UPDRS III, Movement Disorders Society United
Parkinson’s Disease Rating Scale, Part III; NA, not applicable; PDQ-8, 8-item
Parkinson’s Disease Questionnaire; TUG, Timed Up and Go Test; T0, baseline; T1,
immediately after intervention (8 weeks); T2, 3 months after intervention (20
weeks).
a
The control group (group = 1) and the baseline measurement (time = 0) were the
reference categories in the generalized estimating equation model and its
corresponding null variables. b Group effect was defined as group differences at
baseline between intervention and control groups.
c

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 Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease
Time effect at T1 defined as change of scores for control group at T1 compared
with T0; T2 defined as change of scores for control group at T2 compared with T0.
d Group × time effect at T1 defined as additional change of scores for intervention
group compared with control group at T1; T2 defined as additional change of
scores for intervention group compared with control group at T2.
reported significantly greater improvement in MDS-UPDRS
scorescomparedwiththoseintheSRTEgroupduringthestudy
period,thedifferencesinthemeanscoresbetweenthe2groups
wereconsideredtobeclinicallyinsignificant.Thus,MY-PDwas
aseffectiveasSRTEinimprovingmotordysfunctionandmobility, with
additional benefits related to perceived hardship, perceived equanimity,
and HRQOL in people with PD.
TheMY-
PDgrouphadgreaterimprovementinpsychospiritualoutcomes,includinganxie
tyanddepressivesymptoms,perceived hardship, perceived equanimity, and
HRQOL at T1 and
T2comparedwiththeSRTEgroup.Effectsofmindfulnessyoga in improving
psychological outcomes were moderate to large, which has been typical of
evidence-based treatments
recommendedforpsychiatricconditionsofPD.33Thesebenefitswere
remarkable because the participants who received the MY-PD intervention
attended a mean of only 6 sessions.
Both groups showed significant improvement in physical outcomes
related to motor symptoms and mobility, with no statistically and clinically
significant superiority noted. These findings were consistent with the
conclusion of a 2017 systematic review 11 that reported exercise
interventions had beneficial effects on the physical health of patients with
PD.
This study also partially confirmed the findings of another review of
exercise interventions in PD34 that found that physical exercise
interventions had a positive impact on physical and functional capacities,
but there was inconsistent evidence of its effects on nonmotor symptoms
and the psychosocial aspects of life. Integrating mindfulness training into
evidence-based exercise prescription, such as stretching and progressive
resistance exercises,35,36 could be considered in future PD rehabilitation to
optimize patients’ well-being.
Our study findings showed that only the MY-PD group demonstrated
significant improvement regarding the psychospiritual aspects of life.
Mindfulness yoga has been shown to be more effective than conventional
physical exercises for psychological distress management. The noticeable
success of the mindfulness yoga program in improving psychospiritual
well-being confirms the mindfulness component of the interventions.
Mindfulness,amodernBuddhistmeditationpractice,emphasizesthenonju
dgmentalacceptanceofpeopleandsymptoms and the value of being in the
here and now.37 From the Buddhist context, hardship is inherent in life
processes, whereasnonattachmenttopleasuresandhardshipbringsabout
emotional stability. Although the current study is not
intendedtoemphasizeBuddhistphilosophyorreligion,thepatients with PD
who engaged in mindfulness practice
inevitablyexhibitedincreasedspiritualself-care.Thus,theymayhave cultivated
a greater acceptance toward hardship and perceived less hardship and more
equanimity while confronting the vulnerable conditions of PD.
These findings are consistent with the conclusions of various recent
systematic reviews38,39 that reported that mindfulness-based interventions
had beneficial associations with the physical and mental health of patients
with chronic conditions. Through the practice of mindfulness, patients
learn to relate differently to their physical symptoms with a nonjudgmental
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Original Investigation Research
e With log transformation in the generalized estimating equation model.
f
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.
attitude, such that when new symptoms emerge, the consequences are less
significantly disturbing.40,41 In addition to preserving physical and
functional capacities, the mindfulness yoga program appeared to be a
favorable strategy for stress and symptom management among patients
with PD.
Our findings of the increased effects of mindfulness yoga
atT1toT2follow-upregardingpsychospiritualoutcomescontrasted with the
findings of other studies of dance therapy 42 and Qigong43,44 conducted in the
same population. In those studies,thetreatmenteffectsdecreasedatfollow-
up.Thissuggests that mindfulness-based interventions may provide patients
with long-lasting skills effective for stress and symptom management.
Substantial residual gains of mindfulness practices have been reported for
psychiatric treatments. Shapiro and Carlson45 highlighted the dynamic and
evolving natureofmindfulnessskills,whichwouldcontinuetogrowand deepen
alongside practice. Morgan46 found that the residual gains of mindfulness
skills were significantly associated with reductions in anxiety and worry
and with improved HRQOL. The present-focused nature of mindfulness
practice may exertalong-lastingbeneficialeffectasanemotionalcopingskill
tocounterthefuture-orientednatureofanxietyandworryand the past-oriented
nature of depression and rumination.
Althoughtheresidualgainsofmindfulnessskillswerenotmeasured in the
present study, the results highlight the importance of continual mindfulness
practice in daily living.
To complement the subjective self-reported outcomes regarding
psychological distress in the present study, future research should integrate
the use of objective
psychoneuroimmunologicmarkers(suchascortisolandcytokines)toelucidate
the mediating effects of mindfulness yoga on stress and inflammatory
responses in relation to progression of PD. Research to evaluate the long-
term benefits and compliance of mindfulness yoga, identify the reasons for
noncompliance,determinetheminimumdoserequired,andperformcosteffectiv
eness analysis is also necessary.
Compared with other relatively well-established mindfulness
practices, including 8-week mindfulness-based stress reduction and
cognitive behavioral therapy, our mindfulness yoga program adopts a
dynamic exercise approach of mindfulness practice that relies on physical
exertion to achieve physiopsychospiritual benefits. Further research is
needed to compare different approaches of mindfulness practices, for
example, exercise-oriented yoga vs meditation-oriented mindfulness.
Regarding the cultural popularity of various mindfulness practices, a better
understanding of the different mindfulness practices is crucial to enable
patients and health care professionals to select the best practice to optimize
the benefits, satisfaction, adherence, and sustainability for each patient.
Strengths and Limitations
Studystrengthsincludeanassessor-
masked,randomizedclinicaldesignwithlargesampleandadequatestatisticalpo
werto detectaclinicallymeaningfuleffect,multiplefollow-uptime points to
elucidate the residual effects of interventions, involvement of an active
control group, and comprehensive measurement of physiopsychospiritual
outcomes.
(Reprinted) JAMA Neurology July 2019 Volume 76, Number 7 763
 Research Original Investigation Yoga vs Stretching and Resistance Training and Anxiety and Depression in Parkinson Disease
The limitations of this study must be acknowledged. on a unique population of people with mildto-
Expectationbiasmayexistbecauseparticipantswereawareof moderatePDwhoattendedthefollow–upsessions.Allthese
thetreatmentallocation.Selectionbiasmayarisebecausestudy factorsmaylimitthegeneralizabilityofthestudyfindingstothe entire PD
participantswereenrolledthroughconveniencesampling.The population.
volunteersamplemightbemoreactiveinreachingouttocommunityresourcesan Conclusions
dmorewillingtoexercisecomparedwith those who refused to participate or
withdrew from the study. There might be potential bias based on female Among people with mild-to-moderate PD, mindfulness yoga
predominance andearlydropout(n = 15)intheSRTEgroup.Femalesweremore comparedwithconventionalSRTEresultedingreaterimprovement in
interested in receiving mindfulness yoga intervention. Because SRTE was psychospiritual and HRQOL outcomes and had similar benefits on physical
more commonly prescribed for PD outcomes, including motor symptoms and mobility. These findings suggest
rehabilitation,futurecontrolmayincorporatemoreinnovativedesigns, that mindfulness yoga is an effective treatment option for patients with PD
suchasperformingresistancetrainingonanunstabledevice,12 to managestressandsymptoms.ConsideringthatPDisnotonly a physically
toenhanceparticipants’interest,uptake,andadherenceofthe control limiting condition but also a psychologically distressing life event, health
intervention. We purposely excluded people with care professionals should adopt
severePDwhohadseveremotorlimitations,andtheattritionrates aholisticapproachinPDrehabilitation.Futurerehabilitation programs could
of15.2%atT1and18.8%atT2shouldbeacknowledged.Theresults were based consider integrating mindfulness skills into physical therapy to enhance the
holistic well-being of people with neurodegenerative conditions.
ARTICLE INFORMATION Accepted for analysis, and interpretation of the data; preparation, Parkinson’s disease. Neuropsychologia.
Publication: January 11, 2019. review, or approval of the manuscript; and decision to 2018;112:66-76. doi:10.
1016/j.neuropsychologia.2018.03.006
submit the manuscript for publication. 5. Landau S, Harris V, Burn DJ, et al. Anxiety
Published Online: April 8, 2019.
doi:10.1001/jamaneurol.2019.0534 Meeting Presentation: This paper was presented at andanxious-depression in Parkinson’s disease
the 22nd International Congress of Parkinson’s over a 4-year period: a latent transition analysis.
Author Affiliations: School of Nursing, Li Ka Shing
Disease and Movement Disorders; October 6, 2018; Psychol
Faculty of Medicine, The University of Hong Kong,
Hong Kong; and the 15th International Congress of Med. 2016;46(3):657-667. doi:10.1017/
Hong Kong Special Administrative Region (Kwok);
Behavioral Medicine; November 17, 2018; Santiago, S0033291715002196
The Hong Kong Society for Rehabilitation, Hong
Chile. 6. Auyeung M, Tsoi TH, Mok V, et al. Ten
Kong Special Administrative Region (Kwan);
Department of Medicine, Pamela Youde Nethersole Data Sharing Statement: See Supplement 3. yearsurvival and outcomes in a prospective
Eastern Hospital, Chai Wan, Hong Kong Special Additional Contributions: Kenneth Y. K. Wong, MSSc, cohort of new onset Chinese Parkinson’s disease

Administrative Region (Auyeung); Department of
Medicine and Therapeutics, Therese Pei Fong Chow
Research Center for Prevention of Dementia,
Gerald Choa Neuroscience Centre, Faculty of
Medicine, The Chinese University of Hong Kong,
Hong Kong Special Administrative Region (Mok);
Department of Medicine and Therapeutics, Prince of
Wales Hospital, Hong Kong Special Administration
Region (Lau); The Nethersole
School of Nursing, Faculty of Medicine, The Chinese
University of Hong Kong, Hong Kong Special
Administrative Region (Choi, Chan).
Author Contributions: Dr Kwok had full access to all
the data in the study and takes responsibility for the
integrity of the data and the accuracy of the data
analysis.
Concept and design: Kwok, Kwan, Mok, Chan.
Acquisition, analysis, or interpretation of data:
Kwok, Auyeung, Lau, Choi, Chan. Drafting of the
manuscript: Kwok, Kwan, Mok, Chan.
Critical revision of the manuscript for important
intellectual content: Kwok, Auyeung, Lau, Choi, Chan.
Statistical analysis: Kwok, Choi.
Obtained funding: Kwok.
Administrative, technical, or material support:
Kwok, Kwan, Auyeung, Mok, Lau. Supervision:
Kwok, Mok, Chan.
Conflict of Interest Disclosures: None reported.
Funding/Support: This trial was supported by the
Professional Development Fund, Association of Hong
Kong Nursing Staff.
Role of the Funder/Sponsor: The Association of Hong
Kong Nursing Staff had no role in the design and
conduct of the study; collection, management,
City Oasis Mindful Yoga Center; Quentin K. C.
Yau, MSc, BSc, MYO Sports Clinic; Lily M. L. Chan, BN,
RN, North Lantau Hospital, Hospital Authority; and K.
H. Liu, BA, RSW; Carrie S. W. Ha, MSSc, BSS, RSW;
Wing W .Y. Ho, RSW; Eva Q. W. Yip, MSSc,
RSW; and Patsy K. Y. Chan, BSSC, MSW, RSW,
Community Rehabilitation Network, the Hong Kong
Society for Rehabilitation provided expertise and
assistance. The Hong Kong Parkinson’s Disease
Foundation, Hong Kong Parkinson’s Disease
Association, the Association of Hong Kong Nursing
Staff, and the Y. K. Pao Foundation Centre for Nursing
Excellence in Chronic Illness Care provided support to
promote the mindfulness yoga program for chronic
illness management in the community. We thank the
study participants.
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