https://orcid.org/0000-0001-7489-4252
Figures
Abstract
Background
Parkinson’s disease (PD) is a progressive, neurodegenerative disease with motor symptoms that are well understood, but non-motor symptoms may be present and appear at different temporal stages of the disease. Physical activity based on dance movements is emerging as a complementary therapeutic approach to a range of PD symptoms as a multidimensional activity that requires rhythmic synchronization and more neuromuscular functions.
Objective
To evaluate the effects of physical activity based on dance movements on the movement, executive functions, depressive symptoms, quality of life, and severity of PD in individuals diagnosed with PD.
Methods
13 individuals with PD (Hoehn & Yahr I-III, MDS-UPDRS 67.62 ± 20.83), underwent physical activity based on dance movements (2x week for 6 months). Participants were assessed at baseline and after 6 months on movement (POMA, TUG and MDS-UPDRS Part III), executive function (FAB), depressive symptoms (MADRS), quality of life (PDQ-39), and severity of PD (MDS-UPDRS TOTAL). Student’s t-test was used to compare pre and post-intervention results.
Results
We observed a significant improvement in the movement (balance and gait) by the POMA test, p = 0.0207, executive function by the FAB test, p = 0.0074, abstract reasoning and inhibitory control by the FAB, Conceptualization test, p = 0.0062, and Inhibitory Control, p = 0.0064, depressive symptoms assessed by the MADRS test significantly reduced, p = 0.0214, and the quality of life by the PDQ-39 had a significant increase after the intervention, p = 0.0006, showed significant improvements between the pre-and post-intervention periods of physical activity based on dance movements.
Conclusion
Physical activity based on dance movements contributed to significant improvements in movement (balance and gait), executive functions, especially in cognitive flexibility and inhibitory control, and the quality of life too. Sensorimotor integration, most cognitive processing and social skills may have contributed to the results.
Trial registration
The study was registered in the Brazilian registry of clinical trials: RBR-3bhbrb5.
Citation: Duarte JdS, Alcantara WA, Brito JS, Barbosa LCS, Machado IPR, Furtado VKT, et al. (2023) Physical activity based on dance movements as complementary therapy for Parkinson’s disease: Effects on movement, executive functions, depressive symptoms, and quality of life. PLoS ONE 18(2): e0281204. https://doi.org/10.1371/journal.pone.0281204
Editor: Walid Kamal Abdelbasset, Prince Sattam Bin Abdulaziz University, College of Applied Medical Sciences, SAUDI ARABIA
Received: March 31, 2022; Accepted: September 22, 2022; Published: February 2, 2023
Copyright: © 2023 Duarte et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Grant 310054/2018-4, and 447835/2014-9, and 483404/2013-6, and 444967/2020-6, 444982/2020- 5 to Carlomagno Pacheco Bahia), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - Edital n° 21/2018 - Programa Nacional de Cooperação Acadêmica na Amazônia to Carlomagno Pacheco Bahia). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Parkinson’s disease (PD) is the second most frequent neurodegenerative disease in the World and affects around 1% of the global population over 60 years old [1]. It is a systemic disease with a complex clinical manifestation. Beyond the cardinal motor symptoms (bradykinesia, tremor, rigidity, and postural instability), there are non-motor symptoms involving mood disorders, sleep disturbances, cognitive and sensory dysfunctions [2] caused by the neuronal loss in several brain regions together with imbalances in different neurotransmitter systems [3].
The currently available treatments for PD are palliative, do not cover the broad symptomatic spectrum, and do not stop the disease progression [4]. Therefore, non-pharmacologic complementary therapeutic approaches have attracted increasing interest because of their effects on the non-motor symptoms and the quality of life of individuals living with PD.
Physical activity is one of the most widely adopted non-pharmacologic complementary therapeutic approaches for PD, and increasing evidence points to its positive effects on the symptomatic profile [5–9]. In experimental models using small rodents, physical activity reduced risk for the development of PD, improving recovery of motor functions, and neuroprotective effects on dopaminergic neurons [10]. Also, regular physical activity seems to improve neural plasticity through increasing synaptic connections, corticomotor excitation, gray matter volume, and brain-derived neurotrophic factor (BDNF) expression in the human brain [11, 12].
Among the therapeutic approaches based on physical activity such as, for example, physical therapy, aerobic resistance exercises, strength training, and occupational therapy have widely been tested to minimize the progressive development of PD [13–16]. However, more studies are needed to determine the effectiveness of the symptomatic profile [17]. Meanwhile, unconventional approaches such as physical activity based on dance movements, Tai Chi, and virtual reality therapies have been adopted due to specific characteristics that include easy adherence, and compliance, and effects on motor symptoms [18].
There is an increasing interest in the therapeutic applicability of physical activity based on dance movements to the management of neurodegenerative diseases, especially for individuals with PD [19–21]. The physical activity based on dance movements is a multidimensional activity that combines the motor, cognitive, social, emotional, and sensory domains [22]. It may be an excellent way to address motor impairments in individuals with PD through motor stimulation capacities like strength, endurance, flexibility, and functions with neuromuscular demands that include mobility, balance, coordination, and changes in the movement direction [23, 24]. The physical activity based on dance movement demands of cognitive functions through motor learning, memory, creativity, attention, auditory cues, and external sounds rhythmic elements [11, 25, 26]. Additionally, it is considered an enjoyable, motivating, and engaging activity, with good results in adherence for people with PD [27–29].
Therefore, physical activity based on dance movements can be a suitable therapeutic approach to simultaneously address motor and non-motor symptoms of people with PD [30]. Many studies have shown benefits of physical activity based on dance to attenuate symptoms including motor function and quality of life [31]. On the other hand, there are few analyses over non-motor symptoms because the studies are focused on a single aspect of the disease, usually the motor symptoms. Thus, a more throughout evaluation of the beneficial effects of physical activity based on dance movements over the non-motor symptoms of PD need to be explained.
The present study aims to evaluate the effects of physical exercise based on dance movements on the movement, executive functions, depressive symptoms, and quality of life of people with PD. We hypothesize that physical activity based on dance movements may influence the motor and nonmotor symptoms (executive functions, depressive symptoms) and quality of life perception.
Materials and methods
Study design
We performed a longitudinal study aiming to analyze the effects of physical activity based on dance movements as a complementary therapy for Parkinson’s disease on the movement, executive functions, depressive symptoms, and quality of life over six months. The participants performed physical activity based on dance movements using the “Baila Parkinson” method [32, 33], and the global effects were assessed by quantitative tests previously validated for people with PD. This study was conducted at the Laboratory of Studies in Functional Rehabilitation (LAERF), Federal University of Pará, in collaboration with the Laboratory of Neuroplasticity at UFPA located in the Belém, Brazil. Ethics proceedings approval of the present study was awarded by the Ethics Committee for Research in Humans from the University Hospital João de Barros Barreto (proc.n.1338241 CEP/HUJBB/UFPA). The study was registered in the Brazilian registry of clinical trials: RBR-3bhbrb5. The participants provided their written informed consent to participate in this study.
Participants recruitment
The research was developed between May and December 2019. The participants were recruited through social media announcements and subscribed through the research group’s website or telephone. The participants were screened to determine if they met the following criteria: diagnosis according to the UK Parkinson’s disease Society Brain Bank, Hoehn and Yahr stage I to III, under pharmacological treatment for at least 3 years, and on physical conditions to participate in the dance classes. The participants were excluded if they were unable to perform the physical activity based on dance movements, if they had other neurologic or neuropsychiatric conditions, or some comorbidities such as osteoporosis, severe cardiopulmonary diseases, or other conditions that could represent a risk for undergoing physical activities.
Intervention methods based on dance movements
The participants were submitted to two weekly sessions of physical activity based on dance movements (50 minutes/session), in the afternoon for 6 (six) months. The intervention was delivered in the rooms of laboratory and for small groups of 5 to 6 subjects. The rehabilitation program of exercise based on dance movements followed a protocol based on the combination of different dance styles adapted for appropriateness and safety for individuals with PD, named the “Baila Parkinson” method [32, 33].
The “Baila Parkinson” method consists of progressive movement sequences created by combination and adaptation of choreographic elements from different dance styles executed by people with PD in different stages of the disease. The dance styles included: tango, ballroom dance, urban dances, samba, ballet, contemporary dance, and regional dances. The methodology of dance sessions was adapted to compliance and physical limitation by the people with PD. The sessions were structured around the “work lines” of the method, focused on five aspects of the disease, corresponding to the neuropsychological functions affected by PD: cognitive, sensory, motor, emotional and social aspects [34].
Outcome measures
First, we evaluated the people with PD before initiation of the physical activity based on dance movements sessions (pre-intervention) and within the week following completion of the six months of attendance to dance therapy sessions (post-intervention), with approximately 50 sessions performed each patient. Demographic data were collected one week before the first intervention session and included age, sex, time since PD diagnosis, and medications. All patients were tested on the day corresponding the half an hour after taking the antiparkinsonian medication, corresponding to the best ON period of the subject. The tests comprised movement, executive functions, depressive symptoms tests, quality of life assessment questionnaire, and the MDS-UPDRS to evaluation the general symptomatic presentation (Table 1). Test protocols aimed to evaluate the results of the work lines used in the “Baila Parkinson” dance therapy sessions. We evaluated the movement using the Performance Oriented Mobility Assessment (POMA) test [35] focused on balance and gait. Executive functions were evaluated by the Frontal Assessment Battery (FAB) [36]. We assessed the depressive symptoms by the Montgomery-Åsberg Depression Rating Scale (MADRS) [37]. The quality of life was assessed using the Parkinson’s Disease Questionnaire– 39 items (PDQ-39) [38], and finally, the severity of Parkinson’s disease was evaluated by the Movement Disorder Society—Unified Parkinson’s Disease Rating Scale (MDS-UPDRS TOTAL).
Statistical analysis
We performed statistical analysis using GraphPad Prism® 8.0 Software. First, we tested normality (Kolmogorov-Smirnov) and homogeneity (Levine test) of the data. Then we carried out parametric statistical analyses with a paired t-tests to detect differences between the pre-and post-intervention results. The interval of confidence was set in 95% (p<0,05).
Results
Participant characteristics
Twenty-six individuals with idiopathic PD from which eighteen met the selection criteria and were selected to attend the therapeutic sessions (Fig 1). We had 5 dropouts over the study, and only thirteen of the individuals completed the full period of therapeutic sessions. Therefore, only the thirteen subjects that performed the pre-and post-intervention evaluations were included in the current analysis. Demographic data of the analysed participants are presented in Table 2.
Clinical outcomes
Movement tests.
The POMA scores indicated that there was a significant improvement in the balance and gait of the individuals with PD between the pre-intervention (M = 50.77, SD = 5.70) and post-intervention (M = 54.00, SD = 3.49), t (12) = 2.283, p = .0207 when submitted to physical activity based on dance movements (Fig 2A). The POMA test results are shown in Table 3.
Graphic representations of the mean results obtained during the pre-and post-intervention evaluations for the movement (a), executive functions (b), cognitive flexibility (c), inhibitory control (d), depressive symptoms (e), quality of life (f), and Parkinson’s disease severity (g) assessment protocols. Mean ± S.D. t test, * p<0,05 ** p<0,01 *** p<0,001. POMA: Performance Oriented Mobility Assessment; FAB: Frontal Assessment Battery; MADRS: Montgomery-Åsberg Depression Rating Scale; PDQ-39: Parkinson’s Disease Questionnaire—39 items; MDS-UPDRS: Movement Disorder Society—Unified Parkinson’s Disease Rating Scale.
Executive functions test.
In the FAB test, the results obtained in the period before the intervention were as follows: total: 14,3 subdomain conceptualization: 2,23±0,59; subdomain inhibitory control: 1,69±1,18. These values were admitted as baseline for the future measurements. We then observed significant improvement in the evaluation of executive functions after physical activity based on dance movements when compared pre-intervention (M = 14.31, SD = 3.28) and post-intervention (M = 15.69, SD = 2.69), t (12) = 2.840, p = .0074 (Fig 2B). The subdomain of the FAB test, “conceptualization”, indicated a significant improvement in the abstract reasoning between pre-intervention (M = 2.23, SD = 0.59) and post-intervention (M = 2.77, SD = 0.44) when submitted to physical activity based on dance movements, t (12) = 2.941, p = .0062 (Fig 2C). For the FAB test “inhibitory control” subdomain, the results from the pre-intervention (M = 1.69, SD = 1.18) and post-intervention (M = 2.39, SD = 0.77) indicate that the physical activity based on dance movements resulted in an improvement in inhibitory control, t (12) = 2.920, p = .0064 (Fig 2D). The FAB test results are shown in Table 4.
Depressive symptoms tests.
The MADRS test showed a significant improvement in the depressive status between pre-intervention (M = 6.69, SD = 3.79) and post-intervention (M = 4.85, SD = 3.82) intervals, t (12) = 2.264, p = .0214 (Fig 2E). The MADRS test results are shown in Table 5.
Quality of life questionnaire.
The PDQ-39 questionnaire results indicated significant improvement in the quality of life after physical activity based on dance movements when compared pre-intervention (M = 47.19, SD = 16.08) and post-intervention (M = 35.92, SD = 14.40), t (12) = 4.239, p = .0006 (Fig 2F). The PDQ-39 results are shown in Table 6.
Parkinson’s disease severity test.
The Total MDS-UPDRS score showed a decrease in PD severity between the pre-intervention (M = 67.62, SD = 20.83) and post-intervention (M = 64.00, SD = 19.13) periods when submitted to physical activity based on dance movements, however these differences were not statistically significant t (12) = 0.6002, p = .2798 (Fig 2G). The TOTAL MDS-UPDRS results are shown in Table 7.
Discussion
Thirteen individuals from mild to moderate PD participated in 6 months of physical activity based on dance movements, and our results showed improvements in balance and gait, executive function, depressive symptoms, and quality of life. These improvements corroborate the results of previous studies [30, 39, 40]. The participants reported enjoying classes, and 72.2% of those recruited completed the intervention. Here we have demonstrated that regular attendance to sessions of physical activity based on dance movements can improve the clinical characteristics of PD.
Movement tests
The POMA test results showed significant improvement in balance and gait after the physical activity based on dance movements. Previous studies have shown improvement in gait and balance but by independent protocols [28, 30, 41–50]. Only the work by Listewnik and Ossowski [39] evaluated balance and gait by using of POMA test in individuals with PD submitted to 12 weeks of dance therapy whereas in our study physical activity based on dance movements was conducted for six months (approximately 24 weeks) in a larger number of subjects. Both studies found significant changes in balance and gait. The POMA test results showed that physical activity based on dance movements significantly reduced the risk of falls in the evaluated subjects. People with PD have a higher incidence of falls due to balance disorders, slower gait, shorter steps, and usually accompanied by freezing [51]. Physical activity based on dance movements has specific characteristics that can attenuate the motor dysfunctions in the PD such as dynamic balance adjustments and spatial perception, visual and auditory cues, use of music, movements in multiple directions, and rhythmic basis [23]. Audiovisual stimuli can perform greater sensory-motor integration and enhance motor control [52].
Executive functions
Executive functions are the most affected cognitive domain since the early stages of PD [53]. In our study, the participants were in early stages of the disease and the baseline results from FAB tests showed a very mild decline of cognitive executive functions, comparing with results obtained in the same test for people with PD [54]. Some studies have evaluated the effects of dance therapy on the executive functions of individuals with PD and found significant improvement [30, 49]. For the first time, executive functions were evaluated in general and compartmentalized domains to evaluated what executive function specifically showed significant improvement after the physical activity based on dance movements. The results observed may have been achieved from the stimulus provided by our intervention over the executive functions such as cognitive flexibility, inhibitory control, and working memory [55]. For example, new movements and choreographies stimulated cognitive flexibility and inhibitory control by decision-making in movements or choreographic elements not performed impulsively or automatically. Previous studies have shown that dancing reduces the risk of dementia in older people, increases brain white and gray matter volumes, and the concentration of neurotrophic factors compared to other forms of physical exercise [56, 57].
Depressive symptoms
Depression is the most common neuropsychiatric disorder associated with PD. However, often depressive symptoms are neglected in PD due to the difficulty in identifying them and because they overlap with other symptoms of the disease. The significant reduction in depressive symptoms detected by the MADRS test in our study is in agreement with other studies, although performed by different protocols [30, 58, 59]. Before the intervention, 61.54% of our sample had mild depression by the MADRS test. After six months of physical activity based on dance movements, there was a reduction to 23.08% in the occurrence of mild depressive symptoms. Dancing has positive effects on brain regions such as the anterior cingulate cortex and frontal areas [56], brain structures compromised in depression, which may explain the antidepressant effects in the participants of this study [60]. The perceived individual improvement may be a result of the rhythmic and social characteristics of dance, such as the use of music and group sessions which may be able to modulate serotonergic and dopaminergic systems involved in the regulation of mood and motivation, and alterations in these systems are associated with depression and in patients with PD [60–62]. Study participants reported enjoying the classes, a factor that should also be considered since depressed individuals are less active or have high levels of sedentary behavior [63, 64]. We believe that a more comprehensive, in-depth study of this is needed to build on our results.
Quality of life
The results showed a significant improvement in the perception of quality of life, which corroborates the results presented in Albany [40]. The concept of quality of life is complex and multifactorial since several factors influence its perception. Manifestation of motor and non-motor symptoms, side effects of treatment [65], subsequent maintenance, interpersonal relationships, financial, and family life characterize the quality of life in PD. Non-motor manifestations such as depression, anxiety, and psychoses are common in individuals with PD and can also worsen the quality of life [66]. Physical activities like dance movements that focus on physical, motor, emotional and social functions can be a key factor in improving quality of life in several domains. The better the quality of life in PD, the greater the chances of this individual to maintain their functional capacity related to independent living. In addition, we assume that the improvement in the perception of quality of life is a result of the perceived improvement in balance and gait, executive functions, and depressive symptoms in individuals with PD.
Parkinson’s disease severity
Regarding the severity of Parkinson’s disease, our results did not show significant differences in the MDS-UPDRS scores between pre-and post-intervention periods, although other studies have shown the positive results of physical activity based on dance movements approaches over PD progression evaluated by similar tests [30, 40, 44, 67, 68]. One explanation for these results is that, although there are no significant changes in the decrease in PD progression, the fact that our sample did not worsen or remain stable over time is a relevant consideration, as physical activity based on dance movements is an adjuvant approach and reversing or halting disease progression is not intended. Therefore, dance as support to pharmacological treatment is viable, relieving symptoms and improving quality of life.
Limitations
Important limitations of this study must be considered. The first limitation regards the small sample size and the lack of randomization in the design of this study. The very small sample size leads to wide confidence intervals and imprecision in our estimates. The randomization is missing because i) this is a non-controlled study; and ii) participants were free to make the choice of the activity that was being offered, therefore we cannot rule out selection bias, since people with PD who proactively seek adjuvant therapies for PD symptom mitigation may experience different effects of those who are less active.
Also, the use of PD medications was not monitored during the study. Finally, our sample also showed a high standard deviation of the mean scores in the MDS-UPDRS test, which reflects a high difference in PD severity among the subjects. Nonetheless, this study provides important information regarding the outcomes that are most likely to improve with physical activity based on dance movements for people with PD, and also suggests that a larger, randomized controlled trial is warranted.
Conclusion
The present study shows some motor and non-motor benefits from physical activity-based in dance for PD’s patients with significant effects on the balance and gait, executive functions, and depressive symptoms that are positive to the quality of life of people with PD. On the other hand, there were no significant changes in functional mobility and PD severity. Characteristic elements of physical activity based on dance movements such as sensorimotor integration, most cognitive processing, and social skills may have contributed to the results obtained in this study. The paradigm we adopted may be effective in future rehabilitation.
Acknowledgments
We thank all patients, caregivers, collaborators of Parkinson group, Laboratory of Studies in Functional Rehabilitation (LAERF) and to Laboratory of Neuroplasticity (LNP) of the Federal University of Pará (UFPA).
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