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OUTLINE

1. Abstract
2.
3. Keywords
4. List of abbreviations
5. Methods
6. Results
7. Discussion
8. Conclusions
9. Acknowledgments
10. Appendix 1
11. References

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CITED BY (2)

FIGURES (2)

1.
2.

TABLES (6)

1. Table 1
2. Table 2
3. Table 3
4. Table 4
5. Table 5
6. Table 6

ARCHIVES OF REHABILITATION RESEARCH AND CLINICAL TRANSLATION

Volume 5, Issue 3, September 2023, 100276

ORIGINAL RESEARCH
EXPLORING THE EFFICACY OF THE EFFORTFUL SWALLOW MANEUVER FOR IMPROVING
SWALLOWING IN PEOPLE WITH PARKINSON DISEASE—A PILOT STUDY

Author links open overlay panelPooja Gandhi PhD a b, Melanie Peladeau-Pigeon
MHSc a, Michelle Simmons MHSc a, Catriona M. Steele PhD a b
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ABSTRACT

OBJECTIVES

To determine the immediate (compensatory) and longer term (rehabilitative)
effect of the effortful swallow (ES) maneuver on physiological swallowing
parameters in Parkinson disease.

DESIGN

Virtual intervention protocol via Microsoft Teams with pre- and
post-videofluoroscopic swallowing studies.

SETTING

Outpatient hospital setting, with intervention performed virtually.

PARTICIPANTS

Eight participants (median age 74 years [63-82])with Parkinson disease (years
post onset 3-20) with a Hoehn and Yahr scale score between 2 and 4 (N=8).

INTERVENTIONS

ES maneuver, initiated using a maximum effort isometric tongue-to-palate press,
with biofeedback provided using the Iowa Oral Performance Instrument. The
protocol included 30 minute sessions twice daily, 5 days/week for 4 weeks.

MAIN OUTCOME MEASURES

Penetration-Aspiration Scale scores, time-to-laryngeal-vestibule-closure, total
pharyngeal residue, and pharyngeal area at maximum constriction as seen on
lateral view videofluoroscopy.

RESULTS

No consistent, systematic trends were identified in the direction of improvement
or deterioration across Penetration-Aspiration Scale scores,
time-to-laryngeal-vestibule-closure, pharyngeal area at maximum constriction, or
total pharyngeal residue.

CONCLUSIONS

Heterogeneous response to the ES as both a compensatory and rehabilitative
technique. Positive response on the compensatory probe was predictive of
positive response after rehabilitation.

* Previous article in issue
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KEYWORDS

Deglutition
Deglutition disorders
Dysphagia
Effortful swallow
Parkinson disease
Rehabilitation
Treatment outcomes
Videofluoroscopy

LIST OF ABBREVIATIONS

ES
effortful swallow
IOPI
Iowa Oral Performance Instrument
LVC
laryngeal vestibule closure
PAS
Penetration-Aspiration Scale
PD
Parkinson disease
VFSS
Videofluoroscopic Swallowing Studies
Parkinson disease (PD) is among the most common neurodegenerative disorders,
affecting 1%-2% of individuals above age 65, and the fastest-growing neurologic
disease in terms of prevalence, related disability, and mortality.1, 2, 3, 4, 5
Currently, there are no neuroprotective therapies that prevent or delay PD
progression.6 The loss of dopaminergic neurons in the substantia nigra and the
reduction of dopamine concentration in the striatum7 leads to a wide range of
clinical symptoms,8 including motor symptoms of tremor, bradykinesia, and
rigidity.9 Clinical manifestations of PD also feature non-motor symptoms,9,10
including dysphagia (swallowing impairment), which has an estimated prevalence
of ≥40%.11 Dysphagia is largely unresponsive to dopaminergic therapy and
contributes to risk for aspiration pneumonia, malnutrition, and dehydration,
even in the early stages of PD, making timely and efficient management
crucial.12, 13, 14, 15, 16
Dysphagia management commonly includes compensatory measures (eg, postural
adjustments, airway closure maneuvers, diet texture modifications),17,18 but
these have poor patient acceptability and adherence. A recent systematic found
no optimal interventions for dysphagia in PD, however, exercise-based
interventions emphasizing effort and targeting improved swallowing efficiency
showed promise, and visual biofeedback was beneficial.18 Furthermore, a growing
number of studies recommend targeting the physiological mechanisms underlying
swallowing impairment in exercise-based approaches to dysphagia therapy.19, 20,
21, 22 To this end, our group recently conducted a prospective study comparing
swallowing safety, efficiency, timing, and kinematics in individuals with mild
PD to healthy age- and sex-matched controls.19 We identified 2 key mechanisms of
swallowing impairment in PD: (1) prolonged time-to-laryngeal-vestibule-closure
(“LVC”, ie, airway protection), which is a risk for penetration-aspiration of
food and liquid into the airway; and (2) reduced pharyngeal constriction, which
is associated with pharyngeal residue after the swallow. Based on these
findings, we undertook to evaluate a course of dysphagia intervention using the
effortful swallow (ES) maneuver, combining elements of (1) exercise with effort;
(2) experience dependent plasticity (ie, effect of the environment on the
biological organization of the brain); (3) mechanistically targeted treatment;
and (4) external biofeedback. Specifically, the ES was selected as it is
understood to result in greater bolus driving forces and faster bolus transit
secondary to increased amplitudes of oral and pharyngeal muscle
contraction.23,24 Felix et al previously explored the effect of the ES on
impairments in swallowing efficiency and safety in people with PD.25 While they
reported decreased overall residue post intervention, it is important to note
that the authors used clinical judgment to determine the presence/absence of
post swallow residue, rather objective, instrumental methods of measurement.
More recently, a systematic review by Bahia and Lowell concluded that that the
ES leads to increased pressures in the oral, pharyngeal, and esophageal regions,
but the functional effect of the ES in terms of swallowing safety and efficiency
has not been adequately studied.26 They also emphasized the need for
standardization of the ES instructions.
With this in mind, in this manuscript, we report preliminary data regarding the
immediate (compensatory) and long-term (rehabilitative) effects of the ES in a
case series of individuals with PD. We hypothesized that use and repeated
practice of the ES would lead to shorter time-to-LVC and better pharyngeal
constriction, with corresponding functional outcomes of reduced
penetration-aspiration and reduced pharyngeal residue.

METHODS

This study received human subjects approval (CAPCR ID 21-5814). We adhered to
the Strengthening the Reporting of Observational Studies in Epidemiology
(STROBE) guidelines27 for reporting.
Participants were recruited from an outpatient clinic based on the criteria in
table 1. Written consent was obtained. Prior to data collection, participants
were taught the ES as a tongue-pressure emphasis technique, with the instruction
to push the tongue hard against the roof of the mouth and swallow. During this
visit, participants were also taught how to use the Iowa Oral Performance
Instrument (IOPI) and how to thicken thin liquids as per the protocol. Data
collection subsequently began with a baseline videofluoroscopic swallowing
studies (VFSS) to confirm eligibility and probe the compensatory effects of the
ES. Participants who displayed atypical values of prolonged time-to-LVC and/or
poor pharyngeal constriction on regular effort swallows at baseline continued
into a 4-week intervention with two 30-minute sessions of ES practice daily, 5
days/week. The amplitudes of pressures generated when performing the ES were
registered on the IOPI and tracked on a recording sheet by the participant. A
post-treatment VFSS measured rehabilitative outcomes on regular effort swallows.
VFSS ratings were performed according the Analysis of Swallowing Physiology:
Events, Kinematics and Timing for Use in Clinical Practice Method
(https://steeleswallowinglab.ca/srrl/).

Table 1. Inclusion and exclusion criteria used to perform eligibility screening
for participants

Inclusion CriteriaExclusion Criteria
* •
At least 18 years old,
* •
English-speaking,
* •
Able to follow study instructions,
* •
Neurologist confirmed diagnosis of PD,
* •
Hoehn and Yahr scale score of 2 or 3,
* •
Self-report of 1 or more swallowing or related symptoms: a) Difficulty with
secretion management, (b) Coughing at the meal time, (c) Choking on food, (d)
Respiratory infection in the past 6 months (other than COVID).

* •
History of head and neck cancer
* •
Radical neck dissection (eg, anterior cervical spine surgery) or
neck/oropharyngeal surgery (not excluded—tonsillectomy, adenoidectomy)
* •
Past medical history of any neurologic disease other than PD (eg, multiple
sclerosis, amyotrophic lateral sclerosis, traumatic brain injury, stroke)
* •
Cognitive or receptive communication difficulties that precluded the
participant's ability to follow study instructions provided in English. This
was determined by the participant's physician prior to referring them to the
study.

STATISTICS

We adopted a descriptive approach to analyzing the data, by plotting the worst
value for each participant per parameter per consistency on graphs comparing
conditions (ie, baseline regular effort vs baseline effortful; and baseline
regular effort swallows vs post-treatment regular effort swallows). Error bars
were used to illustrate parameter score ranges and an estimated effect size for
each comparison was calculated, by dividing the individual change in scores by
the pooled group standard deviation of worst-scores across the conditions of
interest. These effect size estimates were interpreted according to the guidance
for interpreting Cohen's d, where d=0.2 is considered a “small” effect size, 0.5
represents a “medium” effect size, and 0.8 a “large” effect size.28 Finally, in
addition to the direction of change, the magnitude of change was further
classified based on whether scores moved from the atypical to the typical range,
based on healthy reference values (https://steeleswallowinglab.ca/srrl/).29
Additional details regarding the study methods are available in appendix 1.

RESULTS

PARTICIPANTS

Demographics are presented in table 2. All participants had a neurologist
confirmed diagnosis of PD, with time since diagnosis ranging from 2 to 22 years,
and Hoehn and Yahr Scale scores ranging from 2 to 4. All participants had
self-reported swallowing concerns but none had received any prior swallowing
intervention. Three participants did not qualify for the 4-week intervention
trial: 2 did not show the physiological impairments of interest on the baseline
VFSS, and 1 presented with cognitive impairment limiting her ability to
participate in virtual treatment.

Table 2. Participant demographics

ParticipantAge (y)Sex
Year of PD DiagnosisH&Y Scale ScoreUPDRS Score 2UPDRS Score 3Medication
StateType of Diet/Level of Oral Intake at BaselineMunich Dysphagia Test—PD
ScoreStatus in StudyP174F201421610ONRegular solids and thin liquidsDysphagia
with risk of aspiration
Score: 8.73Baseline and Post-treatment VFSSP282F20192Not availableNot
availableONRegular solids and thin liquidsNot completedBaseline VFSS only; did
not qualify for interventionP374M20143Not available38ONRegular solids and thin
liquidsDysphagia with risk of aspiration
Score: 13.47Baseline and post-treatment VFSSP474F20114Not available54ONRegular
solids and thin liquidsNo noticeable dysphagia
Score: 2.51Baseline VFSS only; did not qualify for interventionP574M20132Not
available35/117*ONRegular solids and thin liquidsDysphagia with risk of
aspiration
Score: 9.01Baseline and post-treatment VFSSP663M201621830ONRegular solids and
thin liquidsDysphagia with risk of aspiration
Score: 6.32Baseline and post-treatment VFSSP765F20004Not available61ONPureed
solids and thin liquidsDysphagia with risk of aspiration
Score: 9.01Baseline and post-treatment VFSSP868M20152Not available23ONRegular
solids and thin liquidsNot completedBaseline VFSS only; did not qualify for
intervention

⁎
Denominator lower because rigidity was not assessed because of online assessment
limitations by MD.

EFFORTFUL SWALLOW AS A COMPENSATORY TECHNIQUE

Figure 1 (panels a–d) provides a graphic overview of the effects of the ES
maneuver when performed as a compensatory technique at the baseline VFSS. The
panels are organized to enable the visualization of functional outcomes of
safety and efficiency on the left side of the figure and the corresponding
mechanistic parameters on the right side of the figure.
1. Download: Download high-res image (719KB)
2. Download: Download full-size image

Fig 1. (a)–(d) Forest plots showing individual participant differences between
regular swallows (squares) and effortful swallows (diamonds) at baseline. Thin
liquid data are shown in white and mildly-thick liquid data in pink. The data
points represent worst scores per parameter for each condition, with the error
bars showing the range of scores seen across 3 task repetitions per condition.
Dashed vertical lines represent the boundary between typical and atypical
scores, based on healthy reference data. Green arrows indicate improvement; red
arrows indicate worsening. Panel a=Penetration-Aspiration Scale scores; panel
b=Time-to-Laryngeal-Vestibule-Closure; panel c=Total Pharyngeal Residue; and
panel d=Pharyngeal Area at Maximum Constriction.

Tables 3 and 4 show the details of change during the baseline VFSS probe of the
ES as a compensatory technique. The relation between changes in
Penetration-Aspiration Scale (PAS)30 scores and time-to-LVC can be appreciated
in figure 1 panels a and b. In panel 1a, participants 2 and 3 showed lower PAS
scores on thin liquids in the ES condition, while participants 6 and 7 showed
lower PAS scores on ES of mildly thick liquids. Of these 4 participants who
demonstrated functional improvement in swallowing safety, 3 showed corresponding
improvement in time-to-LVC on the respective liquid consistencies (fig 1b).
Figures 1c–d capture the compensatory outcomes for swallowing efficiency, with
functional (ie, total pharyngeal residue) and mechanistic (ie, PhAMPC)
parameters shown side by side for each participant. In figure 1c, we see that
all participants except participants 5 and 6 showed improvement in total
pharyngeal residue on at least 1 consistency. Interestingly, of the 6
participants who showed improvement, only 2 showed corresponding improvement in
PhAMPC (fig 1 d).

Table 3. Comparison of Penetration-Aspiration Scale scores between regular
effort and effortful swallows at baseline (thin liquids and mildly thick
liquids)

ParameterConsistencyParticipantRegular EffortEffortfulDirection of
Change*Magnitude of ChangePenetration-Aspiration Scale scores
Thin
IDDSI level 0
P111UnchangedTypical –> TypicalP221LowerAtypical –> TypicalP386LowerAtypical –>
AtypicalP411UnchangedTypical –> TypicalP511UnchangedTypical –>
TypicalP611UnchangedTypical –> TypicalP711UnchangedTypical –>
TypicalP822UnchangedAtypical –> AtypicalMildly-thick
IDDSI level 2P111UnchangedTypical –> TypicalP211UnchangedTypical –>
TypicalP366UnchangedAtypical –> AtypicalP412HigherTypical –>
AtypicalP511UnchangedTypical –> TypicalP621LowerAtypical –>
TypicalP752LowerAtypical –> AtypicalP812HigherTypical –> Atypical

Abbreviation: IDDSI, International Dysphagia Diet Standardization Initiative
framework.
⁎
Lower PAS scores signify change in the direction of improvement; Higher PAS
scores signify change in the direction of deterioration.

Table 4. Comparison of continuous videofluoroscopy measures between regular
effort and effortful swallows at baseline (thin liquids and mildly thick
liquids)

ParameterConsistencyParticipantRegular EffortEffortfulCohen's
d*Time-to-laryngeal-vestibule closure
(milliseconds)
Thin
IDDSI level
0P1132363−1.5P28253633.0P3462561−0.6P43302970.2P52971980.6P6297363−0.4P7231330−0.6P84293300.6Mildly-thick
IDDSI level
2P11321320.0P2198330−0.8P3462594−0.8P4231660−2.6P5165198−0.2P63301321.2P7396991.8P8264429−1.0Total
pharyngeal residue
%(C2-C4)2
Thin
IDDSI level
0P13.10.63.1P22.80.42.9P31.31.20.1P41.30.41.1P511.5−0.6P60.10.2−0.1P70.5Unable
to measureN/AP8000.0Mildly-thick
IDDSI level
2P13.330.1P22.44.9−1.1P33.54.7−0.5P47.16.40.3P52.95.7−1.2P60.80.80.0P72.10.40.7P80.40.30.0Pharyngeal
area at maximum constriction
%(C2-C4)2
Thin
IDDSI level
0P16.22.31.3P20.911.9−3.7P34.35.3−0.3P41.92.2−0.1P51.53.5−0.7P60.61.8−0.4P70.8Unable
to measureN/AP80.200.1Mildly-thick
IDDSI level
2P16.39.6−0.7P2712.8−1.3P37.97.90.0P413.815.3−0.3P54.15.9−0.4P634.5−0.3P76Unable
to measureN/AP80.90.50.1

EFFORTFUL SWALLOW AS A REHABILITATIVE TECHNIQUE

Figure 2 (panels a–d) provides a graphic overview of the effects of 4 weeks of
practicing the ES as a rehabilitative exercise, comparing baseline and
post-treatment VFSS. The panels are organized to show the functional outcomes of
safety and efficiency on the left and the corresponding mechanistic parameters
on the right side of the figure. Tables 5 and 6 show the details of change on
regular effort swallows after 4 weeks of practicing the ES as a rehabilitative
techniques.
1. Download: Download high-res image (620KB)
2. Download: Download full-size image

Fig 2. (a)–(d) Forest plots showing individual participant differences between
regular swallows (squares) and effortful swallows (diamonds) after
rehabilitation. Thin liquid data are shown in white and mildly-thick liquid data
in pink. The data points represent worst scores per parameter for each
condition, with the error bars showing the range of scores seen across 3 task
repetitions per condition. Dashed vertical lines represent the boundary between
typical and atypical scores, based on healthy reference data. Green arrows
indicate improvement; red arrows indicate worsening. Panel
a=Penetration-Aspiration Scale scores; panel
b=Time-to-Laryngeal-Vestibule-Closure; panel c=Total Pharyngeal Residue; and
panel d=Pharyngeal Area at Maximum Constriction.

Table 5. Pre-post comparison of Penetration-Aspiration Scale scores after 4
weeks of practicing the Effortful Swallow (thin liquids and mildly thick
liquids)

ParameterConsistencyParticipantBaselinePost-treatmentChange of
Direction*Magnitude of ChangePenetration-Aspiration Scale Scores
Thin
IDDSI level 0P111UnchangedTypical –> TypicalP386LowerAtypical –>
AtypicalP511UnchangedTypical –> TypicalP611UnchangedTypical –>
TypicalP711UnchangedTypical –> TypicalMildly-thick
IDDSI level 2P112HigherTypical –> AtypicalP366UnchangedAtypical –>
AtypicalP511UnchangedTypical –> TypicalP621LowerAtypical –>
TypicalP751LowerAtypical –> Typical

Abbreviation: IDDSI, International Dysphagia Diet Standardization Initiative
framework.
⁎
Lower PAS scores signify change in the direction of improvement; higher PAS
scores signify change in the direction of deterioration.

Table 6. Pre-post comparison of continuous videofluoroscopy measures after 4
weeks of practicing the Effortful Swallow (thin liquids and mildly thick
liquids)

ParameterConsistencyParticipantBaselinePost-treatmentCohen's
d*Time-to-laryngeal-vestibule closure
(milliseconds)
Thin
IDDSI level
0P1132330−1.8P34623960.6P52972310.6P62971321.5P7231330−0.9Mildly-thick
IDDSI level 2P1132495−2.7P34623630.7P51651650.0P63302970.2P73962641.0Total
Pharyngeal residue
%(C2-C4)2
Thin
IDDSI level
0P13.10.62.9P31.31.7−0.5P511.1−0.1P60.10.2−0.1P70.51.2−0.8Mildly-thick
IDDSI level 2P13.31.21.6P33.54.4−0.7P52.92.40.4P60.80.40.3P72.11.70.3Pharyngeal
area at maximum constriction
%(C2-C4)2
Thin
IDDSI level
0P16.22.81.9P34.32.41.1P51.53−0.9P60.60.9−0.2P70.83.7−1.7Mildly-thick
IDDSI level 2P16.34.60.7P37.99.3−0.6P54.14.5−0.2P632.30.3P768−0.8

Abbreviation: IDDSI, International Dysphagia Diet Standardization Initiative
framework.
⁎
Positive Cohen's d score signifies change in the direction of improvement and
negative Cohen's d score signifies change in the direction of deterioration.
The relation between changes in Penetration-Aspiration Scale scores and
time-to-LVC can be appreciated in figure 2, panels a and b. In panel 2a,
participant 3 showed improved PAS scores on thin liquids, while participants 6
and 7 showed improved PAS scores on mildly thick liquids. All 3 of these
participants showed corresponding improvement in time-to-laryngeal vestibule
closure on the respective liquid consistencies.
The relation between changes in total pharyngeal residue and PhAMPC can be
appreciated in figure 2, panels c-d. As shown in panel c, participants 1, 5, 6,
and 7 showed lower total pharyngeal residue scores post-treatment. Of these
participants, 2 showed corresponding improvement in PhAMPC on the respective
liquid consistencies (fig 2d).

DISCUSSION

The purpose of this study was to explore the preliminary efficacy of a targeted,
effort-based swallowing intervention, both as a short-term compensatory
technique, and after 4 weeks of intensive practice as a rehabilitation technique
in people with PD. Our findings show variability in the direction of change
(improvement and deterioration) for specific parameters across participants and
bolus consistencies. No systematic trends were observed when comparing the
effect of the ES on thin liquid vs mildly thick liquid trials; patients with
earlier vs later onset of PD; mild vs severe PD severity; or related to the
subjective burden of dysphagia as reported on the Munich Dysphagia Test.31 While
changes in either direction did not appear to be predictable, individual
patients did show improvement to varying degrees on particular parameters with
the ES maneuver. All participants who showed improvements on the compensatory
probe in the baseline VFSS maintained or increased those improvements across the
same parameters after 4 weeks of rehabilitation. Additionally, 2 participants
who did not show improvement on the compensatory probe, showed subsequent
improvement at the post-rehabilitation VFSS, and 1 participant with compensatory
improvement showed worse performance on a single parameter post-treatment.
Overall, 4 of the 5 participants who completed the 4-week rehabilitative
intervention showed improvement in 1 or more of the parameters investigated.
The parameters of interest in this study were selected based on hypothesized
physiological and functional relations. Longer time-to-LVC is thought to
contribute to penetration-aspiration, while reduced pharyngeal constriction is
thought to contribute to post-swallow residue,32 both recognized as key
components of dysphagia in PD. As shown in figures 1a-b and 2a-b, this study
provides some support for the idea that time-to-LVC is a key mechanistic
parameter underlying safe swallowing. The strong majority of observed
improvements in Penetration-Aspiration Scale scores (both compensatory and
rehabilitative) occurred in the context of corresponding improvements in
time-to-LVC. Of course, there were also participants whose baseline PAS scores
did not reflect any impairments, and some of these individuals also showed
improvements in time-to-LVC. In terms of deterioration in swallowing, some
participants were observed to evolve from a baseline PAS score of 1 to 2. It is
important to note here that although PAS scores of 1 and 2 are known to occur in
healthy adults, scores of 2 are less common than scores of 1.29 Based on this,
scores of 2 have been considered atypical and heading in the direction of
deterioration (but not reflective of serious clinical concern) in this study.
However, the story is not so clear with respect to changes in swallowing
efficiency. Figures 1c-d and 2c-d do not show a close correspondence between
improvements in total pharyngeal residue and improvements in PhAMPC. Indeed, in
several cases, these 2 parameters showed opposite directions of change in the
same participant. These patterns bring into question the presumed relation
between pharyngeal constriction and residue and suggest that there may be other
mechanisms at play. One factor that may be relevant here lies in the
instructions that were used when teaching the ES. We chose to use a
tongue-pressure emphasis technique, instructing participants to push-off hard
against the anterior palate with their tongues when initiating an ES. This
particular technique may have different effects and yield different results from
ESs where the instructions emphasize greater pharyngeal squeeze or mental
imagery of swallowing a large item such as a whole grape.
The heterogeneous findings in our study may be attributable to variations in
individual participant responsiveness to intensive therapy. This may have been
influenced by a variety of factors, including baseline oral intake status, time
since PD onset, and PD severity. Although we attempted to recruit a homogeneous
sample, with inclusion criteria mandating the presence of specific physiological
impairments, the resulting sample was quite heterogeneous in nature. Despite
these differences, the protocol intensity, duration, and frequency were held
constant across all participants; individualizing the treatment protocol might
have shown different outcomes. Future studies should explore the hypothesized
mechanistic-functional relations between swallowing parameters, across a wider
range of bolus textures, considering additional physiological mechanisms, which
may also affect swallowing efficiency.

STUDY LIMITATIONS

This study was not without limitations. First, this study is a case series with
a small sample size; therefore, caution is warranted when interpreting the
results. A case series design was chosen given expected heterogeneity among
participants, and given the goal of detecting improvements in swallowing
safety/efficiency in a pilot study. However, in this case, where mixed results
were scattered across all parameters in all 8 participants, it is challenging to
derive conclusions regarding cause and effect relations and there is a risk of
over-interpretation.
Second, we only studied participants who were exposed to the intervention. We
acknowledge that comparison to a no-treatment control group would be needed to
make clear inferences regarding intervention effects, The potential for spurious
findings in a small case series justifies a larger, well-powered evaluation.
Third, in order to summarize results across multiple repetitions for each task
and consistency, the “worst” values per task and consistency condition were
captured for each participant. This approach is common in dysphagia clinical
practice, particularly for the Penetration-Aspiration Scale, which has
categorical rather than interval properties.33 However, it is important to
acknowledge that the convention of using worst scores may bias the analysis and
does not account for the variation or frequency of specific scores seen during a
VFSS. Fourth, previous literature suggests significant correlations between
patient-reported subjective experience of dysphagia and PD disease
severity,13,34, 35, 36, 37 and between objective measures of dysphagia and
disease severity.13,35, 36, 37, 38 In this study, we asked patients to report
swallowing-related quality of life using the Munich Dysphagia Test
pre-intervention. This did not reveal correlations with the baseline VFSS
measures of dysphagia or with subsequent improvement/deterioration. In the
future, asking the patients to complete the questionnaire both pre- and
post-treatment would allow for a valuable comparison of perceived change
compared with change on objective VFSS measures. Finally, although a largely
virtual intervention protocol can be beneficial when working with a
neurodegenerative population, the possibility of variability in compliance to
the protocol during home practice sessions exists. In our study, this was
measured through patient/caregiver reports (homework logs), which were returned
at the end of the intervention period. In the future, compliance and home
session fidelity should be examined via home visits, videotaped sessions, or
automatic logging on biofeedback devices.

CONCLUSIONS

Our findings highlight the heterogeneous response to using the ES as both a
compensatory and rehabilitative technique in people with PD. No consistent,
systematic trends were identified in the direction of improvement or
deterioration across penetration-aspiration scale scores, time-to-LVC,
pharyngeal residue, or PhAMPC. This study points to the need for much larger
sample sizes in order to confidently ascertain group-level benefits of the ES
maneuver reinforced with the use of biofeedback, as a therapeutic resource in
the rehabilitation of oropharyngeal dysphagia in people with PD.

ACKNOWLEDGMENTS

The authors gratefully acknowledge financial support from Parkinson Canada in
the form of the Graduate Student Award awarded to the first author, and input
from Emily Barrett and Vanessa Panes regarding stimulus development and
videofluoroscopic rating.

APPENDIX 1

ADDITIONAL DETAILS REGARDING STUDY METHODS

VIDEOFLUOROSCOPY

Videofluoroscopic swallowing studies (VFSS) examinations were conducted at
baseline and after the intervention protocol. These examinations were performed
at 30 frames/s and included boluses of thin and mildly thick liquids as defined
by the International Dysphagia Diet Standardization Initiative framework
(www.iddsi.org). The barium stimuli were prepared using Bracco E-Z-Paque
powdered barium in 20% w/v barium concentration and thickened with a gum-based
thickening agent (Nestlé Resource ThickenUp Clear). Boluses were served in
separate 4-oz cups, each containing 40 mL of liquid. To maximize ecological
validity, participants were instructed to take a comfortable sip and to swallow
when ready, ie, without a cue from the clinician. The baseline VFSS examination
comprised 12 tasks: 3 repetitions of each consistency, swallowed with regular
effort, and 3 repetitions of each consistency performed using the effortful
swallow technique. The post-treatment VFSS comprised 6 tasks: 3 repetitions of
each consistency, swallowed with regular effort.

VIDEOFLUOROSCOPY RATING

The VFSS recordings for each bolus at each examination were relabeled with an
alphanumeric code and assigned to 2 trained raters for independent rating using
ImageJ software (https://imagej.nih.gov/ij/download.html) according to the
Analysis of Swallowing Physiology: Events, Kinematics and Timing for Use in
Clinical Practice Method (https://steeleswallowinglab.ca/srrl/). This standard
operating procedure for rating begins by counting the number of swallows for
each bolus, and scoring swallowing safety on each of those swallows using the
Penetration-Aspiration Scale (PAS).1 The method continues by identifying the
integrity of laryngeal vestibule closure (LVC) seen (complete/incomplete) and
documenting the first-frames of hyoid burst onset, most-complete LVC, and of any
penetration-aspiration events on the initial swallow of the bolus. The parameter
time-to-LVC is then calculated as the difference, in frames, between hyoid burst
and most-complete LVC, and converted to milliseconds based on a frame rate of 30
frames/second. Additionally, pixel-based measures of total pharyngeal residue
and maximum pharyngeal constriction are made using the ImageJ area tracing tool
and normalized to an anatomical scalar defined as the length of the cervical
spine between the anterior inferior corners of the C2 and C4 vertebrae. All
measures were made in duplicate and examined for inter-rater agreement. Exact
agreement was required for number of swallows, PAS scores, and judgments of LVC
integrity. Pre-specified thresholds for inter-rater difference tolerance were
set at >3 frames for frame identification, and >2.4 %(C2-4)2 for area measures.
In cases where inter-rater disagreement fell below these thresholds, rules were
followed to select the earliest of the 2 candidate frames and the smaller of the
2 candidate area measures. In cases where inter-rater disagreement exceeded the
pre-specified thresholds, a consensus meeting was convened for review and
resolution, with a third rater present.

INTERVENTION PROTOCOL

The 4-week intervention program involved two 30-minute sessions of ES practice
daily, 5 days per week. Practice was supervised on a reducing schedule (week 1:
5 sessions; week 2: 4 sessions, etc), via secure videoconference using Microsoft
Teams. Intervention involved biofeedback provided using the IOPI, which was
loaned to each participant for home use. Each session included
* •
15 regular saliva swallows with the IOPI bulb in place.
* •
15 effortful saliva swallows with the IOPI bulb in place.
* •
15 effortful swallows of mildly thick liquid without the IOPI bulb in place,
for generalization.

A homework log was provided to each participant to document the number of tasks
practiced in each session In addition, participants recorded tongue pressure
values as displayed on the IOPI device after regular saliva swallows and
effortful swallows, respectively. The homework logs were used to track
compliance, alongside the supervised sessions.
A supply of thickener was provided to each participant for use in home practice
sessions.
References
1. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A
penetration-aspiration scale. Dysphagia 1996;11:93-8.
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CITED BY (2)

* MANAGEMENT AND TREATMENT FOR DYSPHAGIA IN NEURODEGENERATIVE DISORDERS

2024, Journal of Clinical Medicine

* CORTICAL COMPENSATION MECHANISM FOR SWALLOWING RECOVERY IN PATIENTS WITH
MEDULLARY INFARCTION-INDUCED DYSPHAGIA

2024, Frontiers in Neurology

ClinicalTrials.Gov identification number: NCT05319795.
Disclosures: Catriona M. Steele discloses the following financial relations:
KITE Research Institute—University Health Network (salary); Canada Research
Chairs Secretariat (salary support); Toronto Rehabilitation Institute Foundation
(trainee funding support); National Institutes of Health (grant support
unrelated to this manuscript); Benitec Biopharma (grant support unrelated to
this manuscript); Medbridge (royalties for professional development materials):
Northern Speech Services (royalties for professional development materials);
Nestle Health Science (consulting fees); Bracco Diagnostics (speaker honoraria);
International Dysphagia Diet Standardisation Initiative (speaker honoraria).
Additionally, Catriona M. Steele discloses the following non-financial
relations: Dysphagia Research Society (executive committee member);
International Dysphagia Diet Standardisation Initiative (board member);
Dysphagia Journal (Associate Editor). The other authors have nothing to
disclose.
© 2023 The Authors. Published by Elsevier Inc. on behalf of American Congress of
Rehabilitation Medicine.

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