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PII: S0965-2299(16)30214-X
DOI: http://dx.doi.org/doi:10.1016/j.ctim.2017.03.002
Reference: YCTIM 1667
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1 Highlights
4 • Group therapeutic singing also improves clinical measures of PD as evaluated with the
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5 UPDRS.
6 • Group therapeutic singing may be an engaging early intervention strategy for swallow
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7 impairment in persons with PD.
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1 Therapeutic Singing as an Early Intervention for Swallowing in Persons with Parkinson’s
2 Disease
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6 Department of Kinesiology, Iowa State University, Ames, IA
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7 Department of Communication Sciences and Disorders, Jacksonville University, Jacksonville,
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8 FL
10 Corresponding Author:
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11 Elizabeth L. Stegemöller, PhD
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12 235 Forker Building
14 Ames, IA 50011
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15 esteg@iastate.edu
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16 515-294-5966
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21 Funding Source: This study was supported by the Parkinson Study Group and the Parkinson’s
23 Acknowledgements: We thank Dr. Chris Sapienza for her helpful review of this project.
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1
2 Abstract
3 Objective: For persons with Parkinson’s disease (PD), secondary motor symptoms such as
4 swallow impairment impact the quality of life and are major contributors to mortality. There is a
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5 present need for therapeutic interventions aimed at improving swallow function during the early
6 stages of PD. The purpose of this pilot study was to examine the effects of a group therapeutic
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7 singing intervention on swallowing in persons with PD with no significant dysphagia symptoms.
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8 Design: Cohort Study
13 associated with swallow pre and post the group singing intervention. Swallow quality of life
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14 (SWAL-QOL) and the Unified Parkinson’s Disease Rating Scale (UPDRS) were also obtained
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16 Results: Participants reported minimal difficulty with swallowing, yet results revealed a
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18 total and UPDRS motor scores. No significant differences were revealed for SWAL-QOL.
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19 Conclusion: Increases in EMG timing measures may suggest that group singing results in the
20 prolongation of laryngeal elevation, protecting the airway from foreign material for longer
21 periods of time during swallow. Combined with the improvement in UPDRS clinical measures,
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1
3 electromyography
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5 Abbreviations: Parkinson’s disease (PD); Electromyography (EMG); Swallow quality of life
6 (SWAL-QOL); Unified Parkinson’s Disease Rating Scale (UPDRS); Quality of life (QOL);
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7 Oropharyngeal dysphagia (OPD); High Dosage group (HD); Low Dosage group (LD); Area
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8 Under the Curve (AUC); Analysis of Variance (ANOVA)
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1 Introduction
2 Many non-motor symptoms are common in Parkinson’s disease (PD) which impair
3 quality of life (QOL) and are major contributors to mortality [1-3]. In particular, pneumonia is a
4 leading cause of death in PD [3] and is frequently linked to oropharyngeal dysphagia (OPD) [4],
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5 a symptom experienced by 72%-87% of persons with PD [5]. Signs of OPD can emerge in the
6 early stages of PD, with 40-78% of patients demonstrating changes in swallowing [6-8]. There is
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7 limited research on early intervention for OPD in persons with PD, which is alarming given that
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8 the mean survival time after the significant onset of OPD is only 2 years [6, 9]. Thus, there is a
9 present need for early therapeutic interventions aimed at reducing the impact of OPD and
10 improving QOL. an
11 Measurement techniques related to OPD have ranged from instrumental swallowing
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12 evaluation to patient-reported QOL ratings. Electromyography (EMG) is another promising
14 valid, noninvasive, and does not require exposure to radiation [4]. Previous research has revealed
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15 the effectiveness of EMG for identifying differences in swallow characteristics between PD and
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16 healthy individuals and assessing the effectiveness of training targeting swallowing muscles [10].
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17 Moreover, EMG has been used to characterize swallowing in non-dysphagic patients with PD
18 and EMG results indicate that L-Dopa generally does not impact swallowing function [11].
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19 Overall, the use of EMG in the assessment and treatment of OPD is a promising, yet under-
20 utilized, technique.
22 these treatments have displayed minimal agreement or conclusive utility [12]. Dopaminergic
23 medication is still the primary treatment, but it has not been shown to improve swallowing [4].
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1 Other direct treatments, including exercises targeting the swallowing musculature, expiratory
2 muscle strength training, Video-assisted Swallowing Therapy, surface electrical stimulation, and
3 thermal-tactile stimulation, have shown varying potential for OPD treatment, with more research
4 needed to refine their use [4, 13-20]. Speech therapy, including Lee Silverman Voice training
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5 (LSVT), has also contributed to the treatment of OPD in PD, because of the common
6 musculature for voice and respiration [12], but therapeutic singing has also been proposed as a
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7 viable rehabilitative treatment [21, 22]. Because singing utilizes the same musculature as speech,
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8 it may have a unique combative potential against OPD. Singing offers several additional
9 benefits, namely its memorable nature, ease of self-administration, and potential impact on QOL.
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Yet, research examining the effect of singing on voice and respiration in persons with PD have
11 shown equivocal effects [21, 23-25]. No study has examined changes in swallow function after
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12 therapeutic singing in persons with PD. The development of singing therapies represents a
14 The purpose of this pilot study was to test the effects of an eight-week group singing
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15 intervention on swallow using EMG and swallow-related QOL. Swallow evaluations, the
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16 SWAL-QOL and the Unified Parkinson’s Disease Rating Scale (UPDRS) were completed before
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17 and after the intervention, which was administered in two dosages; once or twice per week. We
18 hypothesized that the singing training would improve swallowing EMG activity and swallow-
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19 related QOL. We also hypothesized that participants who had two sessions per week would show
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22 Methods
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1 Participants/Intervention Overview
3 antiparkinsonian medication regimen completed the study. The diagnosis of OPD was not an
4 inclusion/exclusion criteria for this study; however, no participant was formally diagnosed with
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5 OPD. Participants were excluded if untreated hypertension, history of head or neck cancer,
6 significant cognitive impairment (Mini Mental State Exam score <24), or major psychiatric
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7 disorder (Beck Depression Inventory score <18) were present. Written informed consent was
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8 provided by all participants, and the study was approved by the University Institutional Review
9 Board.
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Participants completed testing and singing interventions while on their normal PD
11 medication regimen. No changes in medication were made throughout the length of the study.
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12 Previous research has demonstrated that medication does not significantly improve EMG activity
13 associated with swallowing in persons with PD [11]. Six participants were placed in a High
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14 Dosage group (HD) that completed two sessions each week; the remaining eighteen participants
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15 were placed in a Low Dosage group (LD) that completed one session each week. To minimize
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16 the potential for drop out due to transportation problems, participants completed the group that
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17 was most feasible for them. Table 1 summarizes participant demographics. The intervention
18 lasted eight weeks, with sessions consisting of various singing exercises to target vocal and
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19 respiratory musculature. All groups followed the same protocol, consisting of warm-up exercises
20 followed by group singing. See supplementary material for a more detailed description of the
21 intervention. Participant enrollment and the intervention methods have been reported in detail
22 elsewhere [25].
23 Pre/Post Testing
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1 The UPDRS, measures of swallow function, and SWAL-QOL questionnaire were
2 collected before and after the intervention. Only participants with PD completed the UPDRS
3 and SWAL-QOL. Caregivers did not assist with the completion of these assessments. The total
4 UPDRS score and motor UPDRS score were summed for each participant. Because neck rigidity
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5 may affect swallow and EMG measures, neck rigidity and swallow scores were obtained for
6 statistical analysis [11]. Higher scores on UPDRS measures indicate more severe impairment.
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7 Swallow function was assessed using surface EMG during three swallows for both the THIN
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8 condition (10 mL of water) and THICK condition (10 mL of pudding). Mean scores were
9 calculated for the THIN and THICK conditions separately. QOL was assessed using the SWAL-
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QOL questionnaire, which is a 44-item questionnaire using Likert-scale ratings to assess QOL
11 related to dysphagia [26, 27]. Scores for each domain were calculated and expressed as a
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12 percentage of the maximum possible points in the corresponding domain. For the total score,
13 each domain score was summed and divided by 10 to produce an overall summary of QOL
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14 related to dysphagia [28]. The first author administered the UPDRS, as she is trained and has
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15 completed this evaluation on many persons with PD. The second and third authors administered
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16 the SWAL-QOL and EMG testing under the supervision of the first author.
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19 EMG (Delsys Trigno) was recorded from electrodes placed over the right and left
20 submental and laryngeal muscle groups (see supplementary material) using The Motion Monitor
21 software (Innovative Sports Training, Inc., Chicago IL) and sampled at 2000 Hz. A low pass
22 filter at 500 Hz, a high pass filter at 1 Hz, and a notch filter at 60 Hz were applied. The raw
23 signal was DC-corrected, full-wave rectified, and smoothed using a root-mean-square envelope
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1 of 50 msec. The EMG signal was manually inspected for artifacts which resulted in a total of 433
2 swallow trials available for statistical analysis. Peak amplitude, area under the curve (AUC), time
3 to peak amplitude, time to onset, time to offset, rise time, fall time and duration were calculated
4 from the resulting curve for both muscle groups (Figure 1).
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5 Peak amplitude was obtained as the peak in EMG activity. AUC was calculated using the
6 trapezoidal rule. For rise time, the duration of the EMG activity from time to onset to time of
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7 peak amplitude was calculated. For fall time, the duration of the EMG activity from time to peak
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8 amplitude to time to offset was calculated. For EMG duration, the duration of EMG activity from
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11 Statistical Analysis
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12 For demographic measures, values were entered into independent t tests to determine if
13 there were differences between groups, except for gender and handedness, in which chi square
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14 tests were completed. For total and motor UPDRS clinical measures, values were entered into
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15 paired t tests to determine changes in clinical measure from pre to post session. Distributions for
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16 neck rigidity and swallow UPDRS scores were not normally distributed, thus the Wilcoxon test
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17 was used to test for differences between pre and post session.
18 Statistical analysis was completed separately for thin and thick swallows and for muscle
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19 groups, similar to previous research [11]. A two-way repeated measures analysis of variance
20 (ANOVA) test was completed for each outcome measure with group and session as independent
22 measures ANOVA for each subdomain and total score. All post hoc comparisons were
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1 completed using Tukey’s Honestly Significant Difference test. All statistical tests were
4 Results
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5 Demographics and Clinical Measures
6 There were no significant differences in demographics between groups for any measure
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7 (Table 1). When comparing across the low and high dosage groups combined, both the total
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8 UPDRS and motor UPDRS scores significantly decreased from pre to post session (total UPDRS
9 reduced by 15%; motor UPDRS reduced by 1%, p < 0.001 for both comparisons). The UPDRS
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neck rigidity score significantly increased from pre to post session (p = 0.03), but there were no
11 significant differences for the UPDRS swallow score. Note that for both of these scores, the
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12 average was less than 1 for both pre and post sessions (Table 2).
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14 EMG Measures
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15 Figure 2 shows EMG data recorded over the laryngeal muscle group from a
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16 representative participant. Observation of the signal suggests that amplitude decreased while the
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17 duration of EMG activity increased from pre to post intervention for both THIN and THICK
18 swallow conditions.
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19 Results for the laryngeal muscle group for both AUC and peak amplitude revealed no
20 significant main effects for session or group for both swallow conditions, and no interaction
21 effects were revealed (Figure 3A and 3C). For the submental muscle group, no significant main
22 effects of session or group or interaction effects were revealed for the THIN condition only. For
23 the THICK condition, no significant effect of group was revealed for AUC but a significant main
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1 effect of session was revealed (F (1) = 4.73, p = 0.04). An interaction effect was also revealed for
2 AUC (F (1) = 5.00, p = 0.04); however, post hoc analysis did not reveal any significant
3 differences. For peak amplitude a significant main effect of session (F (1) = 4.80, p = 0.04) and
4 group (F (1) = 5.66, p = 0.03) was revealed, (Figure 3B and 3D). No interaction effects were
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5 revealed.
6 For the laryngeal muscle group, no significant main effects of group were revealed for
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7 either swallow condition for any of the timing outcome measures (rise time, fall time, EMG
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8 duration), and no interaction effects were revealed. However, significant main effects for session
9 were revealed for both swallow conditions. For rise time, a significant effect of session was
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revealed for the THIN (F (1) = 5.96, p = 0.02) and THICK (F (1) = 7.11, p = 0.01) conditions
11 (Figure 4A). For fall time, a significant effect of session was revealed for the THIN (F (1) =
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12 15.31, p = 0.001) and THICK (F (1) = 13.75, p = 0.001) conditions. (Figure 4C). For EMG
13 duration, a significant main effect of session was revealed for the THIN (F (1) = 39.45, p <0.001)
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15 For the submental muscle group, no significant main effects of session or group were
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16 revealed in either swallow condition for rise time, and no interaction effects were revealed
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17 (Figure 4B). However, a main effect of session was revealed for fall time for both swallowing
18 conditions (THIN: F (1) = 4.73, p = 0.04; THICK: F (1) = 7.80, p = .01). A significant main
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19 effect of group was also revealed for the THICK condition (F (1) = 7.87, p = 0.01), but not the
20 THIN condition. There was an interaction effect for the THIN condition (F (1) = 5.00, p = 0.04),
21 but post hoc analysis revealed no significant differences. There was no interaction effect revealed
22 for the THICK condition. For EMG duration, a main effect of session was revealed for both the
23 THIN (F (1) = 24.59, p < 0.001) and THICK (F (1) = 9.35, p = 0.004) conditions. No main effect
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1 of group or interaction effect was revealed (Figure 4F). Further detail on all statistical results is
4 Quality of Life
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5 No significant main effects for session or group were revealed for the SWAL-QOL total
6 score or any subdomain score. The HD group demonstrated similar total scores of 79.8 ±
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7 10.1(mean ± SD) at baseline to 79.8 ± 15.0 at follow up. The LD group showed similar scores of
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8 84.4 ± 11.5 and 84.2 ± 12.8 at both sessions.
9 Discussion
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Results of this pilot study demonstrate significant increases in EMG timing measures of
11 the laryngeal and submental muscle groups during swallowing in persons with PD after
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12 therapeutic singing. This may suggest that the participants with PD were able to maintain
13 elevation of the laryngeal complex longer, protecting the airway more effectively throughout a
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14 single swallow. These results held regardless of the swallow condition or intervention dosage
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15 group, supporting the hypothesis that EMG activity associated with swallowing would improve
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16 with therapeutic singing, but not supporting the hypothesis that the HD group would demonstrate
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17 greater improvements.
18 This study is the first to examine the effects of singing on swallow in persons with PD.
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19 Targeted exercise therapies (systematic, repeated, and controlled activation of muscles for goal-
20 directed actions) for voice and swallow, including therapies such as EMST and LSVT, have
21 revealed improvements in swallow function [12, 14, 15, 29], but do not target swallowing
22 directly. Rather, they recruit many of the same muscles involved with swallowing [12].
23 Similarly, singing is a goal-directed action that targets specific muscles classifying it as another
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1 form of targeted exercise therapy for swallow. Previous reported results from this study indicated
2 a significant improvement in voice QOL and whole health QOL [25]. Moreover, there was a
3 100% compliance rate for this study, and participants expressed an enjoyment of fellowship with
4 other adults with PD while offering minimal constructive criticism [25]. Taken together with the
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5 significant improvement in both the total UPDRS and motor UPDRS scores reported in this
6 study, therapeutic singing may have additional substantial benefits to persons with PD.
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7 A common cause of swallowing difficulty is decreased hyoid movement [8, 30].
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8 Maintaining elevation of the laryngeal complex and thus the hyoid bone allows the esophageal
9 port to stay open longer allowing more time for the bolus to clear and reducing the chance of
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aspiration. The voluntary prolongation of laryngeal evaluation during swallow, termed the
11 Mendelsohn maneuver, has been used as a rehabilitation exercise for those with OPD [30-33].
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12 Research suggests that the Mendelsohn maneuver increases laryngeal elevation and prolongs the
13 duration of the upper esophageal opening [30, 34]. Other therapies, such EMST, have also
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14 revealed increased laryngeal elevation after training in persons with PD [35]. The results of this
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15 study revealed increases in EMG timing measures suggesting that therapeutic singing may
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16 produce similar effects on laryngeal elevation and may positively impact the timing and
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17 coordination of swallowing. Improving respiratory control may also aid in the prevention of
18 swallow complications, such as aspiration pneumonia in persons with PD [14, 15, 36, 37].
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19 Previously-reported data from this study revealed significant increases in maximum inspiratory
20 and expiratory pressure [25]. Thus, therapeutic singing may be a favorable treatment in
21 combatting OPD and resulting complications by improving respiratory control and prolonging
22 laryngeal elevation.
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1 Previous research has suggested that persons with PD demonstrate longer EMG duration
2 than healthy control subjects as a compensatory strategy due to increased rigidity [11]. UPDRS
3 neck rigidity scores significantly increased from pre to post session in this study. Thus, increases
4 in EMG timing measures may represent an adaptive process to account for neck rigidity.
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5 However, the mean score for the total group was below a score of 1 on a scale from 0 to 4. Thus,
6 neck rigidity was mild in this cohort [38] and may not reliably account for the increase in EMG
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7 timing measures revealed in this study. Nonetheless, changes in rigidity should be considered
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8 when evaluating EMG activity associated with swallow in persons with PD.
9 Mean total scores from the SWAL-QOL did not change from pre to post intervention
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averaging approximately 83 with 100 being the best possible score. Moreover, UPDRS swallow
11 scores were on average less than 1 for both the pre and post session, with a slight decrease from
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12 pre to post session. This score indicates that there may be slowing and increase in effort for
13 swallow, but no reported choking [38]. Given that both the SWAL-QOL and the UPDRS
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14 swallow score are self-reported measures, these results suggest that the PD cohort in this study
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15 did not report substantial difficulty with swallowing. Indeed, none of the enrolled participants
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16 were diagnosed with OPD. Previous research has demonstrated that impairments in swallow are
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17 present even when participants did not notice a significant problem with swallowing, and these
18 can be detected with EMG [6-8, 11]. Thus, increases in EMG timing measures revealed in this
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19 study may indicate a protective beneficial change, even when undetected by the patient. By
20 strengthening muscles and/or limiting the decline of muscle strength, therapeutic singing may be
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23 Limitations
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1 Participants completed the pre and post testing on medication. Every effort was made to
2 schedule the testing sessions at the same time of day such that participants would be in their best
3 medicated state. This was not the case for every participant, and differences in medication timing
4 may contribute to the findings. However, dopaminergic medication has not been definitively
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5 shown to improve swallow in persons with PD [4, 11]. In addition, this pilot study did not
6 include a control group that did not participate in the singing group. The changes in EMG
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7 associated with swallow may be due to other factors present during group interventions.
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8 Placement of the EMG electrodes from pre to post data collection may have confounded results.
9 Every effort was made to place the EMG electrodes accurately and the magnitude of statistical
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difference suggests that other variable may account for differences. Finally, no swallow imaging
11 was completed in this study which limits interpretation of the effects of therapeutic singing on
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12 swallow physiology. There remains is a need for continued research using EMG in assessing
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15 Conclusion
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16 Results from this study suggest that therapeutic singing may improve swallow function
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17 by increasing laryngeal elevation and protecting the airway from foreign material for longer
18 periods of time, and may have additional benefits on other clinical symptoms of PD. These
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19 changes were observed in persons with PD who were not diagnosed with OPD. Previous
20 reported data from this cohort also revealed improvements in respiratory control and QOL [25].
21 Thus, therapeutic singing may be an engaging early intervention strategy to combat OPD and
22 complications such as aspiration pneumonia, while also improving QOL and impacting
23 additional clinical symptoms of PD. These short-term improvements remain clinically important
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1 as PD is a progressive neurodegenerative disease. Future research is needed to determine if
2 therapeutic singing remains beneficial over longer periods of time as disease progressed and
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1 Figure Captions
2 Figure 1. Methods for EMG signal processing. The raw signal is shown in A. The raw signal
3 was DC-corrected and full-wave rectified in B. EMG signal that was above two standard
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5 with a 50 msec window is shown in D. EMG outcome measures are shown in E.
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7 Figure 2. Representative EMG sample from the laryngeal muscle group for one participant for
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8 both thin and thick swallows, pre and post group singing intervention.
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Figure 3. EMG amplitude measures for the laryngeal and submental muscle groups across both
11 groups and swallow conditions. Area under the curve for the laryngeal muscle group is shown in
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12 A, and area under the curve for the submental group is shown in B. Peak amplitude for the
13 laryngeal muscle group is shown in C, and peak amplitude for the submental group is shown in
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14 D.
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16 Figure 4. EMG timing measures for the laryngeal and submental muscle groups across both
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17 groups and swallow conditions. Rise time for the laryngeal muscle group is shown in A, and rise
18 time for the submental group is shown in B. Fall time for the laryngeal muscle group is shown in
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19 C, and fall time for the submental group is shown in D. EMG duration for the laryngeal is shown
20 in E and submental muscle groups is shown in F across both groups and swallow conditions.
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1 References
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5 2. Chaudhuri, K.R., et al., Non-motor symptoms of Parkinson's disease: diagnosis and
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15 26. McHorney, C.A., et al., The SWAL-QOL and SWAL-CARE outcomes tool for
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1 30. McCullough, G.H. and Y. Kim, Effects of the Mendelsohn maneuver on extent of hyoid
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11 35. Wheeler, K.M., T. Chiara, and C.M. Sapienza, Surface electromyographic activity of the
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12 submental muscles during swallow and expiratory pressure threshold training tasks.
14 36. Schultz, J.L., A.L. Perlman, and D.J. VanDaele, Laryngeal movement, oropharyngeal
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1
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MMSE 28.8 ± 1.2 28.9 ± 1.3
BDI 10.3 ± 3.4 7.5 ± 5.0
Education (yr) 16 ± 4 16 ± 2
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Disease Duration (yr) 6±5 10 ± 6
More Affected Side (%R) 50 67
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UPDRS 54 ± 17 59 ± 20
Motor UPDRS 27 ± 11 28 ± 12
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All values are presented as mean ± standard deviation. M = Male; yr = year, R = right; MMSE =
Mini Mental State Exam; BDI = Beck Depression Inventory, UPDRS = Unified Parkinson’s Disease
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6 Rating Scale.
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Total UPDRS** 55 ± 18 47 ± 24
8
ip
Motor UPDRS** 27 ± 11 19 ± 289
UPDRS Neck Rigidity Score* 0.41 ± 0.65 10
0.91 ± 0.93 All values are presented
cr
UPDRS Swallow Score 0.92 ± 0. 93 0.75 ± 0.73
11 as mean ± standard
us
12 deviation. UPDRS = Unified Parkinson’s Disease Rating Scale. Asterisks designate significance. **p <
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