Effects of rhythmic auditory stimulation on functionality in Parkinson’s disease

Introduction: Functionality is affected by the clinical characteristics and progression of Parkinson’s disease (PD). Objective: Assess the effects of a therapeutic exercise program associated with music-based rhythmic auditory stimulation (RAS) on the Activities and Participation Profile (APP) related to mobility of people with PD. Methods: Intervention study investigating people with moderate PD recruited from the Hospital das Clínicas of the Federal University of Pernambuco and the Parkinson’s Disease Association of Pernambuco. The APP related to mobility of the participants was assessed based on the International Classification of Functioning Disability and Health (ICF). The APP contains 23 activity/participation items scored from 0 (no problem) to 4 (complete problem). The intervention consisted of 10 outpatient sessions of a therapeutic exercise program associated with music-based RAS, applied using a smartphone application (ParkinSONS®), performed twice a week, with an average duration of 50 minutes per session. Given the metric nature of the variable and its non-normal distribution, Wilcoxon’s test was applied, considering p < 0.05. Results: In the sample of 8 patients, there was a significant decline in APP scores after intervention (p = 0.018*), indicating a positive change. Scores for all the APP activities decreased following the intervention, except for “transferring oneself to the left side while lying down”. Conclusion: In this study, a therapeutic exercise program associated with music-based RAS had a positive effect on the APP related to mobility of people with moderate PD.

require cognitive and motor skills, in order to improve independence, safety and well-being. 6,8 In PD, the goal of physiotherapy is to maximize functional capacity through movement rehabilitation. 9 Rhythmic auditory stimulation (RAS) with music is increasingly being used as a tool in functional rehabilitation, capable of promoting physiological changes, neuroplasticity and neural circuit reconstruction, thereby contributing to the recovery of motor skills in neurological patients. Research on the performance of the auditory system and rhythmic synchronization in motor control showed synchronization between the auditory and motor systems. [10][11][12][13] Music has the ability to be engaging, emotional, personal, physical, social and persuasive, in addition to promoting movement synchronization, making it a relaxing and enjoyable therapeutic tool. It also provides motor, cognitive, psychosocial and behavioral benefits for people with neurological disorders such as PD, and should be included in multidisciplinary programs aimed at functionality. [14][15][16] Individualized RAS approaches using mobile technology such as smartphone applications may be a safe and economical alternative for outpatient and home-based rehabilitation in patients with PD.
However, the apps currently available are still lacking in terms of providing individualized stimulation suited to the task, with rhythm increases calculated to improve performance. 17,18 No studies were found that assess the effects of physiotherapy protocols associated with music-based The assessment was conducted in the so-called   8. In parallel: walk forwards/ return walking backwards -10 times; to the side and back -10 times, and then walk along a 10-meter-long corridor, turn around and walk back again -10 times. Progression: Walk along a 10-meter-long corridor, 2 sets of 10 laps with a 2-minute rest between sets. Gait training associated with RAS, using songs accompanying training cadence, with an average increase of 10% of the comfortable walking speed 9. Performed after a draw to determine which leg to start with (right or left) and which direction to move in according to the stage of the protocol, which initially consisted of three steps in one direction (step forward-return; step sideways-return; step back-return) 30 seconds with each leg. Progression: six steps in two directions (step back-step forward-return; step back-step sideways-return; step forward-step sideways-return; step forward-step back-return; step back-step forward-return; step sideways-step back-return).
Note: Performed while standing, with the patient supported by a bar or the therapist to prevent possible accidents. The participants were given verbal instructions on correct posture during the exercises, gait and step training.

Results
Sixteen patients were recruited and eight excluded (seven for not meeting the eligibility criteria and one for withdrawing from the intervention in session 8 due to a domestic accident). The final sample consisted of eight patients, most of whom were male and in stage HY2 of the disease. The symptoms of the majority of patients began on the right side of the body (Table 1).
In relation to the APP scores obtained at assessment, participants were classified as "mild problem" in 14 of the 23 items. At reassessment, only the item "transferring oneself to the left while lying down" maintained this classification. All the remaining APP items that obtained "problem" at assessment were categorized as "no problem" after the intervention ( Table 2).
Scores varied from 0 to 2 ("no problem" to "moderate problem") for most of the items. Scores for "transferring oneself to the right and left while lying down", "transferring oneself while sitting" and "squatting" ranged from 0 to 3 ("no problem" to "severe problem"). Only the scores for "walking long distances" varied between 0 and 4 ("no problem" to "complete problem"). Six patients (75%) were attributed a score of 9 (not applicable") for "driving motorized vehicles" and none of the APP items received a score of 8 ("not specified") (  At reassessment, no patients experienced any difficulty for the items "kneeling", "standing", "walking short distances", "waking on different surfaces", "moving around within the home" or "using private motorized transportation" ( Table 3).
The total score of the APP items declined significantly after the intervention (p = 0.018), with only one patient maintaining the same score. The decline in postintervention score varied between 0 and 34 (Table 4).  Table 3 -Percentage of patients with some form of "problem" in APP items before and after the intervention (n = 8 patients)  (14) 14 (14)* Note: APP = Activity and participation profile; x (±) = mean (standard deviation); *p < 0.0001 (Wilcoxon test); n/a: not applicable.

Patient (No.) Total score Score reduction
Assessment (before intervention) Reassessment (after intervention) x (±) 13 (16) 4 (4)* 9 Table 4 -Total score for the 25 APP items per patient (n = 8 patients) before and after the intervention Note: APP = Activity and participation profile; x (±) = mean (standard deviation); *p < 0.018 (Wilcoxon test). The fact that "transferring oneself to the left while lying down" continued to be a "mild problem" after intervention may be related to the protocol's not using RAS for the exercises "rolling over", "bridge" and "upper trunk mobility", which include the mobility needed to perform this activity. Reduced trunk mobility in PD due to axial rigidity is correlated with the difficulty in performing these tasks 2 and is present in the early stages of the disease. 37 Another possibility is a relationship between difficulty with this item and the asymmetry of PD symptoms. The side of the body that patients report as being affected by initial symptoms is generally the most compromised, and in the present study, the right side was the most frequently cited. Patients need good motor control on the right side for "transferring oneself to the left side while lying down". Moreover, as a complex motor skill, this activity is considered difficult and requires the combined mobility of several subcomponents, such as the trunk and upper and lower limbs. 5,38 The use of music-based RAS for transfer exercises in particular could contribute to future protocols, with a view to activating specific pathways in different brain motor areas and releasing biochemical mediators such as dopamine. 34 The intervention had a positive effect on activities related to the exercises used in the therapeutic protocol.
The item "walking long distances", whose scores varied between 0 and 4 ("no problem" to "complete problem") at assessment, improved to "no problem". It is believed that this was largely influenced by gait training associated with RAS, since this strategy seems to promote improvement in gait patterns, such as longer strides

Discussion
In the present study, most of the APP items related to mobility based on ICF exhibited a "mild problem" at baseline assessment in a sample of people with PD. A positive effect was observed for these same items following therapeutic exercises associated with music-based RAS, suggesting that the intervention is a promising strategy for improving the functionality of people with PD and controlling the motor symptoms of the disease.
Exercise programs and training strategies play an important role in improving the functionality and participation of individuals with PD and must be chosen based on careful, comprehensive and individualized assessment of the difficulties they experience. 29 In the present study, we opted for a strategic assessment of the APP by selecting mobility-related activities/participation from the ICF. 25 We believe that this assessment contributed to a better understanding of the effects of our treatment strategy.
At assessment, three activities obtained scores between 0 and 3 ("no problem" to "severe problem"): "transferring oneself to the right and left while lying down", "transferring oneself while sitting" and "squatting".
In a study that investigated women with PD, activities that required consecutive and alternating movements, such as transfers and squatting, were also the most negatively affected by the disease. 30 In PD, changes in the modulation of basal ganglia caused by dopamine depletion result in less cortical activation, which explains the difficulty executing sequential movements and functional tasks. Additionally, axial rigidity is believed to limit trunk mobility and compromise co-contraction of the trunk and hip muscles, reducing selectivity and motor coordination and hampering functional activities. 2,31 The only item with scores that varied between 0 and 4 ("no problem" to "complete problem") was "walking long distances". In a cross-sectional study on functionality, walking limitations were reported by 91% of the individuals with PD in an interview containing items from the ICF. 32 We believe that this finding may be related to compromised spatiotemporal gait parameters caused by the clinical picture of PD, such as shorter stride length, slower walking speed and increased cadence.
Festinating gait and freezing may also be present, associated with postural instability. 31 At reassessment, no patients experienced any difficulty for the items "kneeling", "standing", "walking short distances", "waking on different surfaces", "moving around within the home" or "using private motorized transportation". The lower limb strengthening exercises associated with RAS, in addition to the balance and proprioception training performed in bed, may have favored this finding, since these tasks improve functionality. 42 Step training combined with RAS may also have influenced the postural stability and balance needed for these APP items, since these variables can be improved by including musical rhythm in PD treatment, enhancing the overall stability of postural coordination and optimizing motor function and rehabilitation. 43, 44 A study that used RAS only for step training demonstrated a significant improvement in trunk balance and oscillation, which was maintained for longer (8 weeks) when compared to a group not submitted to RAS, indicating this this stimulus prolonged the effects of step training. 45 The percentage of patients with a "problem" in the "climbing" item remained unchanged post-intervention (25%), which may be because our protocol did not include an exercise compatible with this activity.
Climbing stairs requires significant physical effort 46 and the skills and time needed to perform it have been linked to functional performance and quality of life in people with PD. Studies have found that interventions aimed at improving execution of this task enhance the functional performance of these patients. [46][47][48] Step or stair exercises (climbing up and down) combined with RAS are suggested for future studies.
There was a significant reduction in the total score for the APP items after intervention, with only one patient maintaining the same score. However, it is important to note that the patients studied are constantly monitored, which contributes to good performance. Further research is needed to clarify the effects of an exercise protocol associated with RAS on APP using the ICF, since none that addressed this topic were found. Furthermore, no studies were identified that use ICF items to assess the APP in PD, but rather other instruments commonly applied for functional assessment and included in ICF components. [49][50][51]