Keywords:
dance - Parkinson’s disease - feasibility
Palavras-chave:
dança - doença de Parkinson - viabilidade
In recent years, a growing number of studies on rehabilitation in Parkinson’s disease
(PD) have been published. These protocols have been related to exercise programs aimed
at improving balance, reduction of falls, and cognitive stimulation[1],[2], among others. They also provide various treatment strategies for health professionals,
as well as a new range of activities for patients with PD. This growth might reflect
an overall search for alternative ways of alleviating the symptoms of PD, complementary
to drug therapy[3],[4].
As an adjunct to disease treatment, dancing has become a valuable method of improving
gait, balance, and quality of life (QoL)[5]. Ballroom dancing, especially the tango, has been noted for its high frequency among
the different dance-related rehabilitation practices targeting this population[6]. Several studies on ballroom dancing have shown positive results[7]. However, from a cultural perspective, it may not be an attractive option to all
individuals, and this might lead to withdrawal or reduced adherence to treatment,
which is a major problem often encountered in rehabilitation programs[8].
It is important to create opportunities for patients with PD to take part in different
rehabilitation programs. This will not only help perpetuate these programs, but it
will also ensure that patients encounter different rhythms and steps to promote novel
stimulation of their motor skills[9]. Providing new alternatives with regional characteristics might also be a great
tool for increasing adherence to such activities because patients’ identification
with the music or dance might facilitate their participation in class[10]. Musical familiarity is known to be associated with activation of particular brain
areas, including the motor systems and regions associated with attention and memory[11].
The Brazilian samba is a viable rhythm to be employed as a new dance protocol, because
in addition to targeting motor function through its basic steps, which are similar
to the tango, it targets sensory and social stimulation through its lively pace and
numerous variations in style and music[12]. This rhythm has gained popularity internationally, and it was created and distributed
as “the pace of happiness”[13]; its complexity and quality are direct products of its creation as a collaboration
of intellectuals, scholars, and popular musicians. Overall, samba is a rhythm that
can be played with a variety of different instruments and serves as a symbol of the
joy of its practitioners[14].
Despite the apparent benefits of dance, there are few clinical trial protocols and
feasibility studies, to our knowledge, on the benefits of dance for patients with
PD. A recommendation study on the implementation of a program with tango classes details
the numerous important steps that must be taken for implementing a dance intervention
protocol. However, it does not show the sequence of steps or outline music suggestions[15]. There is also an evaluation protocol of the benefits of ballroom dancing for patients
with PD[5]. Therefore, it is difficult to apply current evidence on the benefits of dance to
clinical practice, as there is no detailed description of the protocol and its validation,
which would be exceedingly important. It is important to investigate carefully the
application of interventions, especially in individuals with PD who rely on a safe
activity and that at the same time provides the physical benefits needed to be then
considered as a tool of rehabilitation.
Based on this background, the objective of this study was to investigate the feasibility
of a Brazilian samba protocol for patients with Parkinson’s disease.
METHODS
This was a feasibility study applied in the first half of 2016 in the city of Florianópolis,
Brazil, using a nonrandomized clinical trial design.
Participants
The sample was selected by individuals diagnosed with PD. They were recruited by telephone
inventory among participants of the Santa Catarina Parkinson's Association (APASC).
Ten individuals (intervention group) agreed to participated in activities in the Pace
and Movement Extension Program of the Health and Sports Sciences Center of the Santa
Catarina State University, in the Santa Catarina Rehabilitation Center (CCR). Ten
individuals agreed to participate in the control group. All participants participated
voluntarily. Altogether, they comprised 20 participants with a mean age of 66.4±10.7
years. The participants were divided in two groups: (a) the experimental group (who
received the dance intervention; 10 participants, mean age=65.30±10.5 years) and (b)
the control group (10 participants; mean age=67.6±10.9 years).
The inclusion criteria were having a clinical diagnosis of PD as per the criteria
of the London Brain Bank[16]; being in mild to moderate stages of the disease; being in the “on” phase of the
medication (assessed through self-reported questionnaire); both female and male participants;
being aged ≥50 years; and not dancing for at least three months.
The exclusion criteria were individuals who had engaged in the practice of any physical
activity or exercise program; who had not completed all stages of the study (75% of
the intervention activities); who had not reached a particular cutoff on the Mini-Mental
State Examination, depending on their education level (13 points for illiterate people;
18 points for average education; 26 points for high schooling)[17]; who were stage 5 according to the Hoehn and Yahr scale[18]; and who had disabilities in daily or social life activities for reasons other than
PD.
Intervention: Classes were conducted by a dance teacher/researcher who had experience
in ballroom dancing, assisted by three other researchers to help minimize fall risks.
For the same reason, we invited patients’ companions to participate in the class,
wherein they closely monitored and assisted participants who had difficulty in executing
certain movements. We instructed them to avoid interfering in the intervention implementation.
Dance protocol
Dance lessons were conducted in a large room that was considered appropriate for patients
with PD. More specifically, it had a floor without deformities and chairs to allow
participants to rest, and the music was set at a moderate volume to ensure that all
practitioners could clearly hear it. Each class lasted one hour, and it was held twice
per week in the evening for 12 weeks following strictly all the steps of Brazilian
samba protocol[19]. The frame with the steps to be taught can be found in the supplementary documents.
Assessments
Data collection was performed by using a questionnaire administered via private, face-to-face
interviews. It was divided into 7 parts: general information; the Hoehn and Yahr scale
18; the Unified Parkinson's Disease Rating Scale (UPDRS)[20]; the Berg Balance Scale (BBS)[21]; and the Parkinson’s Disease Questionnaire (PDQ-39)[22].
Furthermore, in the post-test evaluation, participants were instructed to provide
their perceptions of the magnitude of the perceived changes in their PD symptoms between
the pre and post-test. The values of this measure were used to group participants
and to estimate the minimum clinically important difference (MCDI)[23].
Sample size
We calculated the sample size using G*Power 3.1.9.2. According to an effect size of
0.40, a 5% significance, a power of 95%, and an estimated sample loss of 20%, we expected
that there needed to be at least 20 individuals between the control and experimental
groups[24].
Procedure
This project was approved by the Research Ethics Committee in Human Beings (CEPSH)
of UDESC and by the Brazilian Register of Clinical Trials under protocol RBM82M4D5.
Experimental group
The intervention was held within the Santa Catarina rehabilitation center. The selected
participants were invited to participate in the study voluntarily and take the Brazilian
samba classes. An explanation of the study procedures was given (including the pre-test,
dance classes, and post-test), along with an explanation of the importance of attending
these classes for ensuring health benefits. After agreeing with all steps of the process,
they signed a form indicating their free and informed consent and then data collection
began. A questionnaire was administered before the dance intervention within a two-week
period preceding the intervention (pre-test). Then, the dance classes began; they
were conducted twice per week and each lasted for one hour, according to the study
protocol. After 12 weeks, the post-test was administered in the same manner as the
pre-test.
Control group
The data collection was carried out at the same time as the experimental group. The
researcher scheduled visits to the patients’ residence and clarified the study objectives.
In particular, he stressed the importance of adhering to their current daily activities
and asked them to avoid beginning any new physical activity during the 12-week intervention
period. However, given that mandating a complete abstention from physical activity
for 12 weeks would be inadvisable for preventing diseases and health maintenance,
we emphasized that this was only a guideline.
Furthermore, the control group was invited to attend monthly lectures that would address
the maintenance of health, prevention of falls, and psychological care. They were
asked, in person, about their general health and performance of daily activities.
At post-test (after 12 weeks), participants who had initiated any physical activity
after the pre-test were excluded from the study.
At the end of the study, all participants (control and intervention) received a booklet
containing the main results (including both groups and their own individual results)
in a way that was as clear and objective as possible. Each participant was invited
to continue with the dance activities, as the classes continued after the end of the
study.
[Figure 1] demonstrates the process of selecting participants and performing the study protocol
steps.
Figure 1 Flowchart of the process of subject selection as well as the steps of the study,
2017.
Researchers involved
Data collection was performed by four researchers, all of whom were trained before
the study to ensure that they had the requisite knowledge and mastery of the topic
and its application.
Statistical analysis
We created a database in IBM SPSS Statistics 20.0. Using two-way, repeated-measures
analyses of variance using the Sydak correction for multiple comparisons. The compared
variables included the Hoehn and Yahr scale, UPDRS, BBS, and PDQ-39 score to determine
changes between pre- and post-test in both groups, and to compare the control and
experimental groups at post-test. The significance level was set at 5%.
RESULTS
We first compared the experimental and control groups at the pre-test. We found no
statistical differences between the groups.
At the end of 12 weeks, there was no withdrawal by either EG or CG participants, nor
was there any exclusion from the combined practice of systematic physical activity
concomitant with the study execution time. All participants in the experimental group
performed more than 75% of the proposed activities, as well as in the control group,
that showed 70% of attendance in the monthly lectures offered. The following flowchart
illustrates the process of subject selection as well as the steps of the study:
[Table 1] describes the group’s demographic and general characteristics, where no significant
differences were observed between the groups in any category.
Table 1
Characterization of individuals with Parkinson's disease 2017.
|
CG
|
EG
|
|
n (%)
|
n (%)
|
p-value*
|
|
Sex
|
|
|
1.000
|
|
Male
|
8 (80)
|
8 (80)
|
|
|
Female
|
2 (20)
|
2 (20)
|
|
|
Education
|
|
|
0.062
|
|
Elementary school
|
4 (40)
|
7 (70)
|
|
|
High school
|
5 (50)
|
1 (10)
|
|
|
Higher education
|
1(10)
|
2 (20)
|
|
|
Conjugal state
|
|
|
0.350
|
|
With partner
|
8 (80)
|
5 (50)
|
|
|
Without partner
|
2 (20)
|
5 (50)
|
|
|
Profession
|
|
|
1.000
|
|
Retired
|
8 (80)
|
8 (80)
|
|
|
Active
|
2 (20)
|
2 (20)
|
|
|
Concomitant diseases
|
|
|
0.656
|
|
No
|
5 (50)
|
4 (40)
|
|
|
Yes
|
5 (50)
|
6 (60)
|
|
|
Type
|
|
|
0.171
|
|
Diseases of the circulatory system
|
3 (30)
|
4 (40)
|
|
|
Nutritional and metabolic endocrine diseases
|
2 (20)
|
2 (20)
|
|
|
Socioeconomic status
|
|
|
0.549
|
|
High class
|
2 (20)
|
1 (10)
|
|
|
Middle class
|
6 (60)
|
8 (80)
|
|
|
Low class
|
-
|
1 (10)
|
|
|
Sleeping remedy
|
|
|
1.000
|
|
No
|
4 (40)
|
5 (50)
|
|
|
Yes
|
6 (60)
|
5 (50)
|
|
|
BMI
|
|
|
0.475
|
|
Eutrophic
|
3 (30)
|
2 (20)
|
|
|
Overweight
|
5 (50)
|
8 (80)
|
|
F: frequency; *p-values of exact Fisher test; # Since no differences were found in
the pre and post periods of each group in these variables, we chose to keep only the
data referring to the pre-intervention period.
For all symptom domains, which are presented in [Table 2], there were higher scores after 12 weeks in the control group, thus indicating a
worsening of UPDRS items. Conversely, lower scores after the 12-week dance intervention
were found in the experimental group. When comparing the post-test period between
the two groups, we found that only therapy complications did not achieve a significant
difference (p=0.072). We observed a significant increase in BBS scores (p=0.006) in
the experimental group over the study period, indicating that participants showed
improvement in functional balance. We also observed a significant difference, in BBS
scores between the control and experimental groups at post-test (p=0.045), in favor
of the experimental group.
Table 2
Severity of symptoms and balance of individuals with Parkinson's disease. 2017.
|
Symptoms
|
CG
|
EG
|
|
|
Pre
|
Post
|
|
|
Pre
|
Post
|
|
|
|
|
Ẋ±
|
Ẋ±
|
CS
|
p-value*
|
Ẋ±
|
Ẋ±
|
CS
|
p-value*
|
p-value**
|
|
UPDRS total
|
51.9±6.9
|
62.4±6.2
|
-10.5
|
0.002
|
46.7±21.5
|
34.0±20.5
|
12.7
|
<0.001
|
0.005
|
|
Mental estate
|
5.8±1.0
|
7.0±1.1
|
-1.2
|
0.084
|
4.6±1.0
|
3.6±1.1
|
1.0
|
0.145
|
0.045
|
|
Daily activities
|
16.4±2.0
|
20.5±2.3
|
-4.1
|
0.001
|
15.7±2.0
|
12.5±2.3
|
3.2
|
0.007
|
0.029
|
|
Motor examination
|
22.3±2.9
|
25.1±2.8
|
-2.8
|
0.053
|
20.0±2.9
|
12.0±2.8
|
8.0
|
<0.001
|
0.004
|
|
Complications in therapy
|
7.4±1.5
|
9.8±1.4
|
-2.4
|
0.014
|
6.4±5.8
|
5.9±5.7
|
0.5
|
0.579
|
0.072
|
|
Balance#
|
36.9±4.7
|
37±4.6
|
-0.1
|
0.950
|
49.5±10.7
|
54.0±8.75
|
-4.5
|
0.006
|
0.045
|
X: mean; ±: standard deviation; CS: change scores; UPDRS: Unified Parkinson's Disease
Rating Scale; #Berg's Balance Scale; *p-values of two-way, repeated-measures analyses of variance
using the Sydak correction for multiple comparisons; **post-intervention values between
groups.
As shown in [Table 3], there were no significant changes in the total scores or the scores of each domain
of QoL in the control group. In the experimental group, although the eight domains
and total score of QoL (according to PDQ-39) all declined, only the mobility domain
(p=0.019) showed a significant difference and a large score change (difference of
6.1).
Table 3
Perception of the Quality of Life of Individuals with Parkinson's disease. 2016.
|
GC
|
GE
|
|
|
Pre
|
Post
|
|
|
Pre
|
Post
|
|
|
|
|
PDQ-39
|
Ẋ±
|
Ẋ±
|
CS
|
p-value*
|
Ẋ±
|
Ẋ±
|
CS
|
p-value*
|
p-value**
|
|
Mobility
|
20.2±3.4
|
20.2±3.9
|
-
|
1.000
|
16.7±11.30
|
10.6±11.6
|
6.1
|
0.019
|
0.100
|
|
Daily activity
|
10.4±1.9
|
11.2±2.1
|
-0.8
|
0.571
|
8.4±6.88
|
8.2±6.6
|
0.2
|
0.887
|
0.334
|
|
Emotional
|
10.5±1.7
|
11.8±1.6
|
-1.3
|
0.487
|
10.0±5.9
|
7.3±4.3
|
2.7
|
0.158
|
0.074
|
|
Stigma
|
2.2±1.2
|
2.4±1.1
|
-0.2
|
0.894
|
5.4±5.0
|
4.6±4.2
|
0.8
|
0.595
|
0.197
|
|
Support
|
5.8±0.9
|
4.9±0.7
|
0.9
|
0.357
|
6.0±3.5
|
6.4±1.9
|
-0.4
|
0.679
|
0.170
|
|
Cognition
|
7.2±1.2
|
7.3±1.0
|
-0.1
|
0.936
|
5.9±4.8
|
4.7±2.9
|
1.2
|
0.342
|
0.106
|
|
Communication
|
2.7±0.7
|
3.1±0.7
|
-0.4
|
0.462
|
2.6±2.5
|
2.1±2.3
|
0.5
|
0.360
|
0.360
|
|
Discomfort
|
5.3±0.5
|
5.5±0.9
|
-0.2
|
0.789
|
5.5±1.6
|
5.1±3.3
|
0.4
|
0.594
|
0.775
|
|
Total
|
64.3±7.5
|
66.4±9.3
|
-2.1
|
0.757
|
60.5±27.7
|
49.0±27.9
|
11.5
|
0.103
|
0.206
|
X: Mean; ±: standard deviation; CS: change scores; UPDRS: Unified Parkinson's Disease
Rating Scale; #Berg's Balance Scale; *p-values of two-way, repeated-measures analyses of variance
using the Sydak correction for multiple comparisons; **post-intervention values between
groups.
At the end of the 12-week intervention, all experimental group participants reported
a feeling of improvement in the studied symptoms, with five participants reporting
little improvement, three reporting significant improvement, and two reporting very
significant improvement.
Feasibility aspects
During class implementation, there were no falls, which is a very important aspect
of what is a safe activity to this population. The presence of the assisting researchers
was essential for both aiding students who found it more difficult to perform certain
movements and maintaining a climate of contagious positive stimulation and encouragement.
All dance activities adhered to the details of the protocol steps without any changes
to the suggested sequence, which indicated that the participants were able to perform
all the dance steps.
Adherence and non-users
Considering the absences and non-compliance in certain tasks, patients completed,
on average, 82.7% of activities. According to the eligibility criteria, at the end
of the intervention, patients must have been present for 75% of activities; after
12 weeks, we observed no cases of exclusion on this basis, which strengthens our hypothesis
that the protocol can be useful for improving patient adherence to a rehabilitation
program.
Problems
Since most participants were male, a very important aspect of achieving successful
completion of the intervention was encouraging participants’ companions to participate
in the classes to prevent participants from performing an activity without a partner.
The researchers also took part in some of the dance classes, partnering with participants,
to stimulate participants and increase their safety when performing movements that
are more complex.
DISCUSSION
The aim of this study was to examine the feasibility of a Brazilian-samba intervention
protocol for patients with PD. The samba protocol adopted in the study can be considered
viable for individuals with PD. We found that the applicability of the classes, the
progression of content, the acceptance and maintenance of participants, the safety
of the activities, and the improvement in symptoms after interventions were viable[23].
All dance activities observed in this study followed the steps outlined in the protocol
without any deviations, which demonstrates that the participants were able to perform
all the steps and that the progression of activities was appropriate for patients
with PD. This orderly sequence of activities is necessary to stimulate patients’ motor
skills and adaptability to new situations, which are important for patients with PD
to deal with the fluctuations arising from the disease[15]. The series of steps were chosen to maintain a steady flow, which consists of an
intrinsically surrounding mental state that occurs when there is a perception of balance
between the individual's ability and the demands of the activity[25], thus adding with patients’ engagement in the activity, decreasing their negative
perceptions, and increasing perceptions of performance by them[26].
If the proper precautions are taken, this intervention appears to be a reliable tool
for rehabilitation of PD because, during the twelve-week intervention period, there
were no falls. Shanahan et al.[9] notes that falls pose a significant risk to the health and physical integrity of
patients with PD, and furthermore can be extremely discouraging for them; once a patient
has experienced a fall, they might become ashamed to return to classes. As such, balance
is an important factor in adherence to PD interventions[27] and should be prioritized when conducting lessons. Therefore, it is important that
a team assists the lessons, as they can help in patients’ execution of movements,
such as by improving patients’ security, as well as stimulating patients’ confidence
via words of encouragement and motivation; these efforts can in turn promote patients’
confidence in the activities[8].
Another positive aspect of this protocol was the fact that 82.7% of participants adhered
to the activities, and that 100% completed the intervention; in other words, there
were no withdrawals during the 12-week period. This shows that the activities were
enjoyable, which encouraged participants to remain in class. Furthermore, the low
number of absences ensured the continuous positive progression of activities, and
excellent adhesion can help improve participants’ social relationships with class
members. This is because regularly attending an activity that stimulates interaction
with other people can help participants create social ties, which is often impaired
with the advancement of the disease[27].
Although this will not be a study to analyze cause and effect of the practice of dance,
the statistical analysis indicated that the intervention was very effective in improving
the scores assessed by the UPDRS. While the scores in the control group showed a negative
change, we observed positive changes in all domains and the total score in the experimental
group. For patients with a progressive neurodegenerative disease such as PD, maintaining
the symptom scores can be considered a gain, since the disease shows a natural worsening
of symptoms - as was observed in the control group[28]. In this case, however, the intervention went beyond mere maintenance for some symptoms
- in fact, it improved them. These results reinforce the hypothesis that the samba
can, as well as in other interventions already performed with dance in individuals
with DP, become a tool for these individuals’ rehabilitation, including memory stimulation,
improvement of daily activities execution, as well as body control improvement and
motor skills of such activities[8],[27],[29],[30]. These effects can directly benefit the day-to-day activities of these individuals,
as they are closely linked with functional independence. Researchers have shown that
cognitive and motor deficits are commonly associated with greater dependence on cariers[30], thus being able to slow down the progression of symptoms of PD is a major advance
for patients with the disease[29].
Despite the importance of UPDRS maintenance, one of the sought-after outcomes of dance
interventions is improvement in functional balance[31],[32]. Dances take place through natural movements and uses music to stimulate practitioners[33], thereby leading to better results even when compared with other physical activities[34]. The improvement in functional balance scores was clear in this study. A likely
cause of this improvement is the characteristics of the basic steps of the samba.
Since they involve continually stepping forward and backward, as well as whirling
in place, they might stimulate motor schemas, and when performed rhythmically can
activate cortical areas to improve motor skills and individuals’ balance[8].
One of the aims of the intervention was to observe if as well as in other dance interventions,
the samba could improve the patients’ QoL; however, despite improvements in the eight
domains and overall QoL, only one domain (mobility) showed a significant change. The
QoL results coincide with the findings of Heiberger et al.[35], who also used the PDQ-39 and found that the motor problems showed greater improvements
than did the QoL of motor skills. These values are justified by the subjectivity of
QoL assessments, which makes it difficult to measure accurately QoL changes unlike
more objective tests such as the BBS. It is important to highlight the differences
in PDQ-39 changes between the control and experimental groups - namely, all control
group scores showed negative changes, thereby indicating deterioration in QoL, whereas
experimental group scores all showed positive changes. There is consensus that the
PD progression influences patients’ QoL[36], these results indicate a trend that dance can have a positive influence on participants’
QoL. Another fact that may have influenced this result was the absence of a group
activity on the part of this control group; it is well known that the practice of
collective activities can improve aspects of QoL mainly in the social aspects[37].
Although the QoL and motor symptoms were highlight results in intervention studies,
the clinically important differences of perceived changes have been increasing importance,
especially in interventions with individuals affected by any disease[23]. All practitioners mentioned feeling some form of improvement in their symptoms
after the 12-week intervention. As noted above, while dance can influence motor skills,
it is nevertheless important that patients realize this change, as it would lead to
improved health awareness and self-esteem and automatically in the search continues
to maintain its activity. Indeed, perceived physical ability is one factor that appears
to influence adherence to practical interventions for PD[27].
This study showed a decline in scores well above the values commonly found in the
literature for the control group. Still, despite that all the individuals in the control
group practice physical therapy, the activity has not been controlled, not being perhaps
applied effectively to bring the minimum benefits for this population.
This study presents limitations. One of them is the non-randomization design, even
though being the design chosen and following all the steps proposed by the protocol,
it is known that randomization can avoid research bias, as the choice of individuals
to participate or not to dance classes can baseline the group and influencing the
outcome. However, these limitations are less of an issue since this is a feasibility
rather than an efficacy trial.
Thus, it is concluded that the samba protocol for individuals with PD is viable. It
brought numerous benefits in the studied variables, in particularly, it has proven
to be safe and can provide enough physical benefits, as well as lead to improvements
in social relations. The execution of this protocol activity as an alternative to
non-pharmacological therapy that can be used simultaneously to the pharmacological
treatment, in addition to showing possible tools for the maintenance of individuals
in intervention programs. It is also a possible adherence tool of participants in
certain intervention programs and a promise for efficacy in future clinical trials.
