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Effect of Lee Silverman Voice Treatment (LSVT LOUD®) On Swallowing and Cough in Parkinson's Disease
Effect of Lee Silverman Voice Treatment (LSVT LOUD®) On Swallowing and Cough in Parkinson's Disease
A R T I C L E I N F O A B S T R A C T
Keywords: Purpose: Lee Silverman Voice Treatment (LSVT LOUD®) is an effective therapy for phonation in Parkinson's
LSVT LOUD® Disease (PD) but little is known about any additional spread of effects to swallowing and cough function. This
Dysphagia pilot study examined the effect of LSVT LOUD on pharyngeal swallowing parameters and reflexive cough
Swallowing strength.
Voice
Methods: Twenty participants (14 men, 6 women; mean 68 years, SD3.5) with PD referred for LSVT LOUD with
Parkinson's disease
complaints of voice deterioration were recruited. Mean duration of PD was 6 yrs., SD 3. Self-reported Eating
Cough
Assessment Tool-10 scores ranging from 0 to 25 (normal < 3). Prior to LSVT LOUD, 1-week post- and 6-months
post-treatment, participants undertook a videofluoroscopic study of swallowing and aerodynamic measures of
involuntary cough.
Results: All participants completed the LSVT LOUD programme; 3 participants were lost to follow-up at 6-
months. All participants made significant gains in average sound pressure level (dB SPL). Aspiration was not
observed. Pharyngeal residue (p < 0.05) and pharyngeal area at rest reduced (p < 0.01) while maximal
opening of pharyngoesophageal segment (PES) (p < 0.05) and PES opening duration (p < 0.05) significantly
increased. There was a significant improvement in involuntary cough peak expiratory flow rate and peak ex-
piratory flow rise time. All changes were maintained at 6-months.
Conclusion: LSVT LOUD demonstrates additional spread effects on pharyngoesophageal deglutitive function and
involuntary cough effectiveness in people with mild PD referred with voice complaints. Consequently, LSVT
LOUD has potential to provide additional benefits for swallowing safety and efficiency in this patient group.
Abbreviations: VFSS, videofluoroscopic study of swallowing; TPT, Bolus transit time [total pharyngeal transit time; AEdur, airway closure duration maximum; Hdur, hyoid displacement
duration; AEcl-BP1, airway closure time (AEcl) in relation to bolus reaching PES (BP1); PESdur, pharyngoesophageal sphincter (PES) opening duration; PAhold, pharyngeal area at rest;
Hmax, maximum hyoid displacement; HL, hyoid-larynx displacement; PESmax, maximal opening of the pharynoesophageal sphincter; PCR, pharyngeal constriction ratio; CPD, com-
pression phase time; PEFR, peak expiratory flow rate; PEFRT, peak expiratory flow rise time; CVA, cough volume acceleration; EMST, expiratory muscle strength training
⁎
Corresponding author at: School of Psychology, Tamaki Campus, The University of Auckland, Private Bag 92019, Auckland, New Zealand.
E-mail address: a.miles@auckland.ac.nz (A. Miles).
https://doi.org/10.1016/j.jns.2017.11.015
Received 30 May 2017; Received in revised form 23 October 2017; Accepted 14 November 2017
Available online 15 November 2017
0022-510X/ © 2017 Elsevier B.V. All rights reserved.
A. Miles et al. Journal of the Neurological Sciences 383 (2017) 180–187
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A. Miles et al. Journal of the Neurological Sciences 383 (2017) 180–187
2.5. Acoustic speech protocol participant was asked to perform a dry swallow to see if clearance oc-
curred. At 60 s, screening was terminated irrespective of presence of
Speech measures were taken as per the LSVT LOUD standardized residue to limit radiation exposure in keeping with the local policy.
protocol: sustained vowel (/a/), maximum phonation time (MPT)
(maximum phonation value recorded of three attempts), average
reading dB SPL (“Rainbow Passage”) and average conversation dB SPL 2.7. Aerodynamic protocol
(2 min) [21,23,33]. A sound level meter (CEL-244 Class 2, Casella) was
calibrated with a CEL-110/2 Acoustic calibrator, and was placed on a Strength of reflexive cough was calculated using ADInstruments™
tripod 30 cm away from the participant's lips. LSVT LOUD sessions were Spirometry (Bella Vista, Australia) coupled to a nose covering face-
conducted in a quiet room in participants' own homes, without back- mask with a side delivery port linked via a one-way valve to a
ground noise. Voice signals (dB SPL) were recorded throughout each PulmoMate Nebuliser model 4650I (DeVilbiss Healthcare LLC,
session and averages were later calculated. Assessors were blinded to Pennsylvania, US). LabChart™ software from ADInstruments™ recorded
the participants' previous scores. cough flow parameters. Reflexive cough was elicited once using 0.8 M
citric acid [a supramaximal concentration expected to trigger a re-
flexive response in the majority of adults [35]], vaporized through the
2.6. Videofluoroscopic study of swallowing mask with the instruction “cough if you need to”. The nebulizer was
stopped after three successive coughs or after 30-s if no cough occurred.
VFSS studies were performed in a radiology suite using a
Videofluoroscope (DF-323H, Toshiba, Japan) and were recorded at 30
frames per second onto USB drive. Timing information was super- 2.8. Quantitative measures
imposed on the fluoroscopic recording in 100ths of a second using a
Horita VS-50 Video Stopwatch (Horita, California USA). A 20 mm All measures were completed by one of two authors who were not
diameter radio-opaque ring was taped to the patient's chin (in the lat- involved in the participants' LSVT LOUD programme. Both authors
eral plane) and shoulder (in the anterior-posterior plane) to allow ca- were experienced in aerodynamic and videofluoroscopic quantitative
libration for displacement measures. A Medical Radiation Technician measures. They were given all de-identified data at the end of data
(MRT) and an experienced speech-language pathologist participated at collection and were blinded to participant and time point.
all procedures. In the lateral plane, the patient was presented with Each videofluoroscopic study of swallowing was analysed using
20 ml of thin liquid barium (E-Z Paque 96% w/v diluted to 19%) fol- ‘Swallowtail’ [Version 1 (2016), BellDev Medical, IL]. Each swallow
lowed by 100 ml of thin liquid barium through a straw with the in- was rated using the eight-point penetration-aspiration scale where
struction “drink the whole cup in your own time but without stopping”. 1 = no penetration/aspiration and 8 = aspiration below the vocal
The participant was then given 5 ml of barium paste (E-Z-paste 60%w/ cords with no attempt to clear [36]. Residue was measured as flat
w). The same sequence was administered during VFSS per participant. surface area of residue (using 1st frame after epiglottis returns to rest
Bolus textures and volumes were trialled once and used so that mea- position) using the area measuring tool in Swallowtail. Swallow studies
sured data could be compared to previously published normative data were measured quantitatively using validated parameters (Table 1)
[29,34]. These also represent commonly swallowed texture con- derived from the protocol published by Leonard and Kendall [29].
sistencies as produced by mastication of foodstuffs. Screening captured These parameters have proven sensitive to subtle changes in swal-
the oral cavity, pharynx, upper esophagus and upper airway. Studies lowing physiology in both healthy and dysphagic subjects [37,38].
were truncated if significant aspiration or coughing occurred. No Twenty-percent of VFSS videos were randomly selected using a random
prompting was provided to swallow or cough during the protocol. In number generator for measurement by a second rater. Inter-rater re-
the anterior-posterior plane, the participant was positioned standing liability across all measures was strong [ICC (3,1) > 0.85] [39].
and asked to “swallow all in one go” (to avoid deglutitive inhibition) a Cough recordings were measured on the first cough in the reflexive
20 ml bolus. The bolus was followed from the oral cavity through to the cough sequence (Table 2) [40]. Twenty-percent of cough recordings
lower esophageal sphincter. Screening was continued for up to 15 s. If were randomly selected using a random number generator for mea-
there was still residue in the esophagus, screening was ceased for 15 s, surement by a second rater. Inter-rater reliability across all measures
then recommenced for another 15 s. If residue was still present, the was strong [ICC (3,1) > 0.95] [39].
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A. Miles et al. Journal of the Neurological Sciences 383 (2017) 180–187
Table 1 LOUD and six months post-LSVT LOUD for each dependent variable
Oropharyngeal measures of timing, displacement, and area [29]. using an adjusted p value (adjusted alpha level = 0.05/5 repeated
tests = 0.025) given the repeat testing. Where assumptions were vio-
Measure Description
lated, Friedman test was used with post hoc analysis using Wilcoxon
Bolus transit time (seconds) signed-rank test.
B1 Onset of bolus transit Associations between motivation scores and acoustic speech mea-
BP2 Tail of bolus clears UES
sures were calculated using Spearman's Correlation (2-tailed) test re-
Total pharyngeal transit time BP2 – B1
(TPT) Total time of bolus passage through ported with means and standard deviations.
the pharynx Two-way mixed, single measures intra-class correlation coefficients
Swallow gesture times (seconds) for absolute agreement (ICC3,1) were used to calculate the intra- and
AEs Airway begins to close inter-rater reliability of the experienced raters. The Cicchetti inter-
AEc Airway is closed
pretation of ICC estimates was used to determine the strength of
H1 First movement of hyoid towards
displacement agreement: poor (0.00–0.39), fair (0.40–0.59), good (0.60–0.74), and
H2 Hyoid is maximally displaced excellent (0.75–1.00) [39].
H3 Hyoid begins to return to resting
position
3. Results
Pop UES first opens
PESmax UES is at its maximum opening
Pcl UES closes Twenty participants with PD received LSVT LOUD treatment (14
Em Epiglottis returns to upright position male; mean 69 yrs., SD9.0, range 50–83; 6 female; mean 64.5, SD8.7,
Airway closure duration (AEdur) Em – AEc range 49–76). Mean UPDRS was 25, range 9–48, SD11 with a mean
Total time airway is closed during
duration of PD of 6 yrs., range 1–15, SD 3. All participants took med-
the swallow
Pharyngoesophageal sphincter (PES) Pcl – Pop ications for their PD and none had received deep brain stimulation. All
opening duration (PESdur) Total time UES is open during the participants were assessed pre- and one week post-LSVT LOUD; three
swallow participants were lost to follow-up at six-months due to logistics with
Maximum hyoid displacement duration H3 – H2
travel to the radiology suite. All participants reported eating a normal
(Hdur) Total time hyoid is maximally
displaced during the swallow
diet with no modifications to fluids or food; however eight participants
Displacement measures (cm) (40%) scored outside the normal range (> 3 points) on their pre-
Maximum hyoid displacement (Hmax) Distance between hyoid at rest and treatment EAT-10 suggesting some early swallowing disturbances
maximally displaced within the group (Table 3). No changes in medical status, physical ac-
Hyoid-larynx displacement (HLmax) Distance between hyoid and larynx
tivities or medications were reported during the study. No additional
at rest and maximally approximated
Maximal opening of the PES (PESmax) The maximum opening of the UES speech therapy was provided between the LSVT LOUD treatment and
Anatomical measures (cm2) the six-month follow-up. However, all participants had been re-
Pharyngeal area at rest (PAhold) Area of Pharynx at rest commended to continue practising daily as per LSVT LOUD protocol.
PAmax Maximal constriction of pharynx
PAmax/PAhold Pharyngeal Constriction Ratio (PCR)
3.1. Motivation, PDQ-8, EAT-10 and acoustic speech outcomes
Table 2 All participants completed the full treatment programme. Ten par-
Aerodynamic measures [40]. ticipants were given a score of 5 out 5 for their motivation and com-
mitment to their LSVT LOUD programme and homework completion
Measure Description with eight participants receiving a 4 and only two participants receiving
Compression phase duration peak inspiratory flow during the inspiratory
a score of 2. Motivation rating was not significantly associated with
(CPD) phase of the cough speech outcomes: maximum phonation time (MPT) (R = 0.42,
Peak expiratory flow rate (PEFR) peak airflow during the expiratory phase of p = 0.067), average reading dB SPL (R = 0.30, p = 0.20) or average
the cough conversation dB SPL (R = 0.28, p = 0.23).
Peak expiratory flow rise time time from the beginning of the expiratory
There were significant increases in MPT, average reading dB SPL
(PEFRT) phase to the peak expiratory flow
Cough volume acceleration expiratory peak flow/expiratory phase rise and average conversation dB SPL one week post-LSVT LOUD
(CVA) time (p < 0.001). This was maintained six months post-LSVT LOUD for
MPT and average reading dB SPL (p < 0.01) but not average con-
versation dB SPL (p = 0.32). PDQ-8 (p < 0.01) and EAT-10
2.9. Data analyses (p < 0.001) significantly reduced across time with a significant dif-
ference between pre- LSVT LOUD and one week and six months post-
Descriptive statistics were compiled. Data were compared to pre- LSVT LOUD; with no significant change between one week post-LSVT
viously published normative data for videofluoroscopic swallowing LOUD and six months post-LSVT LOUD (Table 4). Of the eight parti-
parameters [29] and voluntary cough parameters [40,42]. Statistical cipants who scored outside of the normal range for EAT-10 pre-treat-
analyses were completed using SPSS Version 23 (SPSS, Chicago, IL). An ment, six participants improved their scores (range of score reduction
Intention-to-treat analysis approach was taken using data from all 3–18), one remained the same, and one scored themselves three points
participants including the three participants lost to follow-up at six- higher than pre-treatment.
months. Missing data points were managed using single mean im-
putation. Each dependent variable, measured at the three time points, 3.2. Videofluoroscopic study of swallowing measures
was analysed using repeated measures ANOVA (with a Greenhouse-
Geisser correction where sphericity assumptions were violated). A No instances of aspiration occurred (all boluses scored 1 on the
p < 0.05 was considered statistically significant for all ANOVA ana- penetration/aspiration scale) consistent with the participants' mild PD
lyses. presentation. Pre-LSVT LOUD, only three swallowing measures were
When the ANOVA was significant (< 0.05), Bonferroni post hoc more than 1SD outside of previous normative data: AEdur, PCR and
tests were completed to determine significant changes between pre- PESmax [29].
LSVT LOUD and one week post-LSVT LOUD and between pre-LSVT While nine participants (45%) had PESmax opening more than 1SD
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Table 3
Participants' demographic information and self-reported Parkinson's disease severity scores.
Age (years) Gender Duration of UPDRS (0 = no PDQ-8 (0 = no impact of EAT-10 (0–3 = normal Working Other activities
PD (years) disability, 199 = worst symptoms, 100 = maximum range, 40 = worse
disability) impact) difficulties)
Table 4
Self-rating scales and speech outcomes pre-, post- and 6-months post-LSVT LOUD.
Mean, SD p value
Pre- LSVT LOUD Post- LSVT LOUD 6 months post- LSVT LOUD Statistic
PDQ-8 (raw score out of 40) 12.55, 7.11 10.50, 4.82⁎ 10.55, 4.96⁎ F 6.29, p < 0.01
EAT-10 (raw score out of 40) 10.55, 4.95 4.10, 5.31⁎ 4.2, 5.91⁎ X2 18.03 p < 0.001
Maximum phonation time (secs) 13.93, 6.47 17.40, 5.72⁎ 20.74, 14.28⁎ X2 7.15 p < 0.05
Average dB SPL reading 66.16, 4.77 73.71, 5.72⁎ 71.89, 3.68⁎ X2 25.05 p < 0.001
Average dB SPL conversation 65.99, 4.04 71.11, 4.43⁎ 64.6, 17.55 X2 16.69 p < 0.001
⁎
Statistically different from baseline pre-LSVT LOUD.
below the normative data pre-therapy, this had reduced to only three 4. Discussion
participants post-LSVT LOUD. There was a significant increase in PES
opening duration and PES maximum opening during ingestion of the This study assessed the additional swallowing-related effects of
20 ml fluid bolus between pre-LSVT LOUD and one week post-LSVT LSVT LOUD in those already attending treatment. Patients were se-
LOUD. Improvements were maintained at six months. lected based on meeting voice treatment criteria for LSVT LOUD irre-
There was a significant reduction in residue with the paste bolus spective of their swallowing difficulties. Self-reported overall PD
between pre-LSVT LOUD and one week post-LSVT LOUD that was symptoms and self-reported swallowing symptoms improved after
maintained at six months post-LSVT LOUD (p < 0.05). Only one par- treatment. Data demonstrated significant reduction in pharyngeal area
ticipant had a PCR outside of 1SD from the norm and this did not reach at rest suggestive of improved overall pharyngeal tone, significantly
normal range post-LSVT LOUD. There was a significant decrease in improved pharyngoesophageal inlet opening duration and improved
pharyngeal area (cm2) at rest across time with a significant decrease PES opening diameter. These parameters are associated with improved
between one week post-LSVT LOUD and six months post-LSVT LOUD as pharyngeal bolus transit, reduced pharyngeal residue and therefore
well as between pre-LSVT LOUD and one week post-LSVT LOUD reduced post-deglutitive aspiration risk [29]. There was also a sig-
(p < 0.05) (Table 5). nificant improvement in involuntary cough peak expiratory flow rate
Although airway closure time (AEdur) between time frames did not and peak expiratory flow rise time. Most importantly, the improve-
reach statistical significance (p = 0.08), the number of participants ments documented here were sustained at six months following LSVT
who fell more than 1SD outside of the norm, reduced from seven to one LOUD treatment.
participant after LSVT LOUD.
4.1. Swallowing parameters
3.3. Aerodynamic cough measures LSVT LOUD is a validated therapy for hypophonia. As has been
shown previously, participants in this study achieved greater loudness
All participants produced an immediate multiple cough sequence in and maintained gains after the treatment period [20]. LSVT LOUD is
response to the citric acid. A number of participants exhibited abnormal non-invasive and intensive. Primary treatment aims include improving
cough measures pre-treatment with 70% of participants measured to be respiratory drive to the larynx and recruiting muscles that support
more than 1SD outside of the norm for PEFR [42] (Fig. 2). phonation. These activities are also crucial in deglutitive function. One
There was a significant improvement in PEFR and PEFRT but not previous study found improvement in oropharyngeal transit time and
CPD or CVA between pre-LSVT LOUD and post-LSVT LOUD (Table 6). residue following standard LSVT LOUD treatment [28] but evaluated a
PEFR and PEFRT improvements were maintained at six-months. small sample size with measures of bolus timing and residue only.
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A. Miles et al. Journal of the Neurological Sciences 383 (2017) 180–187
Table 5
Videofluoroscopic measures pre-, post- and 6-months post-LSVT LOUD.
Paste (5 ml)
⁎
Residue (cm2) 0.16, 0.26 0.09, 0.18 0.09, 0.22⁎ F 4.9 p < 0.05
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A. Miles et al. Journal of the Neurological Sciences 383 (2017) 180–187
misdirected bolus (compensating for reduced swallowing safety). there is a need to develop other treatment options and to minimize
Seventy percent of participants performed below normal range in their patient risk and discomfort. The possible side effects of medication and
reflexive cough PEFR. Although changes in CPD (a measure of glottal the risks of surgery are completely avoided using this rehabilitative
closure) and CVA (a measure of cough effectiveness) did not reach intervention. LSVT LOUD has been proven to reap greatest results in
significance, PEFR and PEFRT significantly improved. The 12% im- people with mild-moderate PD and requires a reasonable level of cog-
provement in PEFR across the cohort has been demonstrated to corre- nition, motivation and stamina [54]. This study offers promise in pro-
late with clinically relevant change in people with asthma [46]. The tecting these people against life-compromising swallowing and re-
high-effort respiratory tasks in LSVT LOUD perhaps heighten re- spiratory difficulties suffered later in PD. It is possible that in patients
spiratory drive for the forced expiratory task of reflexive cough. Similar already suffering from more significant swallowing dysfunction and
concurrent changes in expiratory cough measures and swallowing airway compromise, who are still cognitively able to participate in the
safety have also been seen following expiratory muscle strengthening rigorous programme, that the effects of LSVT LOUD may have an even
training (EMST) where a patient expires forcefully into a calibrated greater protective effect and a recalibration of the whole sensorimotor
device [47–50]. process [23]. Further investigation is warranted.
The frequent interaction of patient with therapist during LSVT LSVT LOUD demonstrates additional spread effects on quantitative
LOUD may have a bearing on perceptual responses. Motivation ratings pharyngoesophageal deglutitive function and involuntary cough effec-
were high in the majority of participants. Frequent encouragement with tiveness in people with mild PD referred with voice complaints. This
specific direct feedback can enhance motor learning and bolster moti- offers promise in protecting against the respiratory and deglutitive
vation [23]. This supportive effect may play a role in the perceived symptoms suffered by people with mild PD in a non-invasive manner.
benefit of therapy leading to improved perception of PD symptoms However, LSVT LOUD is not a replacement for direct swallowing
(PDQ-8) and swallowing symptoms (EAT-10) despite the participants' treatment for this population at this time. This pilot data justifies a
treating clinician not being involved in the assessment sessions. Im- randomized controlled study to understand whether the identified
provement in quantitative measures are, however, beyond the partici- benefits can be found in those with more severe PD and dysphagia and
pants' control. Participants were blind to the measures that were being to assess overall duration of benefit.
assessed and therapy focuses on speech only. This reduces the risk of
approval bias whereby the patient is seeking approval from the clin- Declarations
ician for achieving certain outcomes.
The study cohort was small, non-randomized and without a control, The authors have no conflicts of interest to declare. This project was
with follow up limited to only six months. It should be noted that the supported by a Neurological Foundation Project Grant and a Maurice
use of multiple LSVT LOUD clinicians increases risk of variability in Phyllis & Paykel Trust Project Grant.
treatment delivery. Now that we have clear evidence of benefit, a larger
randomized controlled study will be performed, with a control group to Acknowledgements
assess natural variability over time. An accurate power calculation can
now be made based on the significant changes in residue, timing, dis- Thank you to the participants of this study for their enthusiasm,
placement and/or pharyngeal area in this pilot work. Further in- support and participation. We would also like to acknowledge
vestigation of the correlation between functional outcomes and quan- Waitemata District Health Board for their support, LSVT LOUD-certified
titative swallowing and cough measures in a large, more impaired speech-language pathologists Sharon Broadmore, Sharon Farao and
sample will add clarity to physiological mechanisms of change. Future Louise Hume as well as the continuing support of Miriam Maslin,
considerations include a longer duration of follow up, to identify Medical Radiation Technician, Radiology, Waitemata District Health
whether drop-off in function occurs and if repeating LSVT LOUD would Board and Alex Hunting and The University of Auckland speech pa-
demonstrate repeated effect or cumulative improvement. Participants thology students for contributions to assessment and measurement.
were recruited solely through the LSVT LOUD service secondary to
complaints of voice dysfunction. Future studies will expand on these References
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