Keywords deglutition disorders - Parkinson disease - endoscopy - cognition
Introduction
Dysphagia can significantly affect the quality of life of people with Parkinson disease
(PD); it is a risk factor for aspiration pneumonia, the leading cause of death in
patients with PD.[1 ]
[2 ]
[3 ] Dysphagia is very common in PD, affecting over 70% of patients.[4 ] The specific swallowing difficulties most frequently associated with PD are found
in the oral and pharyngeal phases, resulting in abnormal bolus formation, delayed
swallowing reflex, and prolonging pharyngeal transit time.[5 ]
Deglutition disorders generally require good care, and can lead to dehydration and
malnutrition in patients with PD,[6 ]
[7 ] in addition to aspiration syndromes. Gastrointestinal symptoms are common even before
the onset of PD motor symptoms, even though patients recognize their difficulties
later.[8 ] Parkinson disease can affect any phase of the swallowing process (preoral, oral,
pharyngeal, or esophageal), as well as the adjacent respiratory, olfactory, and salivary
systems, due to slowed movement execution, restricted range of motion, reduced physical
strength, and, most likely, impaired perception.[9 ] Oropharyngeal dysfunction can occur during the early stages of the disease, and
is characterized by repetitive swallowing (double or triple) for a single bolus, due
to esophageal peristalsis deficits.[10 ] It is plausible that dysphagia can remain subclinical or asymptomatic as patients
gradually adapt to it as a consequence of the slow progression of PD.[11 ] The loss of somatosensory input leads to silent aspiration attributable to the accumulation
of non-identifiable residues in the oropharyngeal region.[12 ]
The fiber optic endoscopic evaluation of swallowing (FEES) is considered the gold
standard test for the diagnosis and management of swallowing disorders, minimizing
the risk of aspiration.[13 ] This test involves fiber optic examination of the pharynx and larynx, the swallowing
of various food substances under endoscopic visualization, and the response to therapeutic
maneuvers.[14 ]
Tasks that require simultaneous performance of two or more functions (walking and
talking on the phone, or walking while repeating a shopping list, for example) may
be particularly difficult for patients with PD. Specific cognitive aspects, such as
subdividing or alternating attention, have been specifically associated with impairment
to perform two tasks simultaneously. Studies on simultaneous tasks involving locomotion
are more common in the literature, and their main objective is to understand and prevent
falls in patients with PD.[15 ]
[16 ] Evidence suggests that patients, while in locomotion, should focus their attention
on the act of walking, thinking about each step and reducing automation in their movements
while discontinuing simultaneous tasks.[17 ]
However, few studies have highlighted the effect of dual tasks on swallowing.[18 ]
[19 ] A study[18 ] that analyzed swallowing of 10 mL of a liquid viewed through video fluoroscopy concurrently
with the memorization of numbers showed that both tasks were impaired when they were
performed simultaneously. In other words, swallowing was impaired when it was performed
along with a cognitive task. Despite cognitive-motor interference, the patients with
greater impairments regarding cognition and attention demonstrated improved swallowing
safety under a dual-task condition.
A comprehensive understanding of the mechanisms that influence deglutition under dual-task
conditions is important to address concerns regarding feeding safety. The act of swallowing
occurs in a social environment with motor competition, such as movement of the hand
and arm to take food to the oral cavity, for example. The present study tested the
hypothesis that performing concurrent tasks could decrease the safety of swallowing
in PD patients as visualized using the FEES.
Methods
The present study was approved by the Ethics in Research Committee (approval under
number 1.008.61) of our institution.
Participants
The present is an interventional, case-control study, and it was conducted by dividing
the subjects into two groups. One group included patients with PD. The group composed
of healthy controls (HCs) included individuals who were matched for chronological
age, gender, and level of schooling.
A significance level of 5%, power of 90%, and a standardized effect size of one standard
deviation in the results of the 2 evaluations (isolated and double task) were used
to assess correlations in at least 13 individuals in each group. The calculation was
performed using the freeware package WinPepi, version 11.43, and was based on the
study by Brodsky et al.[19 ] The survey sample was expanded to 19 PD patients and 19 HCs.
The PD patients were sorted at the Parkinson clinic of the reference hospital in Brazil.
All evaluations were performed while the patients were receiving antiparkinsonian
drugs and during the “on” phase.
Visitors to the otorhinolaryngology ward were included in the control group. These
individuals were matched for gender, chronological age (considering ± 4 years), and
level of schooling (considering 5 years of schooling as the cut-off).
Inclusion and Exclusion Criteria
The patients who met the following criteria were included in the PD group: 1) willingness
and ability to provide informed consent to participate in the study; 2) previously-confirmed
diagnosis of PD; 3) no self-reported history of swallowing difficulty; 4) absence
of motor impairments that could prevent manual tasks; 5) presence of the hand movement
skills necessary for the study; 6) absence of any malformation and/or surgery involving
significant resection of tissues or the laryngeal structure or reconstruction of the
larynx; 7) absence of any disease causing stunting of the esophagus and of the esophageal
surgery tract; and 8) no reconstruction surgery of the esophagus and/or any associated
neurological disorders.
For the HCs, the inclusion criteria were the same except for the diagnosis of PD.
Scales and Procedures
The patients with PD were classified by a neurologist according to the Hoehn &Yahr
(H&Y) Scale,[20 ] which classifies PD in terms of the degree of severity of the symptoms. All subjects
included in the study underwent a brief cognitive assessment by an expert using the
Mini Mental State Examination (MMSE)[21 ] and the Montreal Cognitive Assessment (MoCA).[22 ]
Fiber Optic Endoscopic Evaluation of Swallowing (FEES)
Experimental procedures for dual tasks were performed in the hospital using video
nasoendoscopy. The FEES examination was performed using the protocol described by
Langmore et al.[23 ] The characteristics of the apparatus used for fiber optic nasal endoscopy included:
a 3.2-mm flexible Machida ENT-III scope (Madrid, Spain), a Xenon Storz (Tuttlingen,
Germany) light source, a Storz video monitor, an R170 Samsung (Seoul, Korea) DVD recorder,
and a 4.7-GB DVD-R Maxprint (São Paulo, SP, Brazil) envelope. The images were recorded
on CDs for further analysis and interpretation.
Functional swallowing tests were compared using the Boston Residue and Clearance Scale
(BRACS), which has been validated by Kaneoca et al[24 ] and is specially designed for studies involving FEES. The BRACS enables the functional
analysis of residue considering three variables: volume, location, and patient response.
Therefore, the analysis is based on the following criteria: 1) amount and location
of the residue; 2) spontaneous clearing during swallowing; and 3) clearing effectiveness
of swallowing. Based on this information, a total score is established. Two trained
researchers compared the scores of volumes offered under the isolated-swallowing condition
and under the dual-task condition. In cases in which there was disagreement, a third
examiner performed the classification. The examiners were blinded to the patients
and controls.
The BRACS is an 11-point ordinal scale that measures the severity of a residue problem.
The scale specifically defines the amount of residue (none/coating; mild = covering/filling < 1/3
of the location; moderate = covering/filling between 1/3 and 2/3 of the location;
and severe = covering/filling > 2/3 of the location). The amount of residue is scored
in 12 locations of the laryngopharynx. An extra point is added if residue is noted
in four or more anatomical regions. An additional point is added if the residue is
present inside the vestibule, placing the individual at the highest risk for aspiration
after swallowing. If residue is observed and the individual demonstrates no spontaneous
clearing swallows, an extra point is added to account for the apparent lack of pharyngeal
sensation. Cued or spontaneous swallows are then judged for effectiveness (yes = 80%
to 100% cleared; partially = 20% to 80% cleared; no = 0% to 20% cleared).[24 ]
Experimental Procedures
The participants were instructed as to the procedures at each stage of the examination:
isolated swallowing; manual movement; and isolated swallowing and manual movement.
After comprehending the tasks, the test began. Each task was interspersed by a rest
period during the supply of food. The patients were instructed to stay at home and
wait for the offer of new food. The offers of 3 mL and 5 mL of food were made in isolated-swallowing
and dual-task sequences.
Swallowing: both groups underwent the FEES examination with 3 mL and 5 mL of moderately
thick food classified according to the International Dysphagia Diet Standardization
Initiative (IDDSI) as level 2[25 ] in the syringe stained in blue, which is considered a safe consistency and volume
for patients. The examination was performed by an ENT physician, and the food was
offered by a speech therapist. The patient was positioned in a chair facing the ENT
doctor and was asked to perform the previously practiced procedures.
Dual task: After the patient performed the procedures with the food being administered
by the researcher, the protocol was repeated for IDDSI level 2 of fluid with the patient
performing opposition of the thumb concurrently with swallowing, the dual-task condition.
The hand movements used were opposition of the thumbs in sequence of 1-3-4-2, in which
the numbers correspond to: 1 - index finger; 2 - middle finger; 3 - ring finger; and
4 - pinkie. The order of presentation of the tasks was standardized for all patients.
Analysis of the Results
The statistical analysis was performed using the Statistical Package for the Social
Sciences (SPSS, IBM Corp., Armonk, NY, US) software, version 20.0. For the comparisons
of the association of single or dual tasks with the BRACS for each group, we applied
the Mann-Whitney test. For the comparison of dual and single tasks and the 3 mL and
5 mL volumes for each group, we applied the Wilcoxon test. The paired t -test for independent samples was used for the statistical comparisons of means between
the groups. For the intersection of data between the H&Y, MoCA and MMSE variables,
the Spearman correlation coefficient (rs ) was used.
Results
The PD and HC groups consisted of 19 subjects with a mean age of 61.5 and 60.8 years
respectively. Most of the subjects were men (68.4%). The mean level of schooling was
of 8 years for the PD group and of 10 years for the HC group, as shown in [Table 1 ].
Table 1
Demographic variables of the study sample
Variables *
Parkinson disease patients
Healthy controls
p -value
(n = 19)
(n = 19)
Age (years)
61.5 ± 7.1
60.8 ± 8.7
0.792
Gender
1,000
Male
13 (68.4)
13 (68.4)
Female
6 (31.6)
6 (31.6)
Schooling (years)
8 (5–11)
10 (6–15)
0.191
Mini Mental State Examination
24.6 ± 4.9
26.7 ± 2.6
0.120
Montreal Cognitive Assessment
22.6 ± 6.1
21.8 ± 4.5
0.676
Note:*Data expressed as mean ± standard deviation, median (25–75 percentile) or n
(%).
The patients recruited were between H&Y stages 1 and 4. Of the 19 PD patients, 12
were classified as stage 2, 6, as stage 3, and 1, as stage 4. [Table 1 ] summarizes the demographic information of all participants.
The present study compared two conditions: isolated swallowing and swallowing under
the dual-task condition with 3 mL and 5 mL of food. All participants performed the
proposed tasks safely and successfully completed the evaluation. There was a statistically
significant difference regarding the results of swallowing alone and of the dual task
assessment between the two groups. The highest scores were found in the PD group for
both tasks and volumes. The median score of the PD subjects for the 3-mL volume was
2 for swallowing and 4 for the dual task, while the median scores were significantly
lower among the HC subjects. The same variation was observed for the 5-mL volume,
with a median score in the PD group of 2 for swallowing and 4 for the dual task, while
the median score was 0 for swallowing and 1 for the dual task in the HC group, as
shown in [Table 2 ]. When comparing the performance of the individual task versus the dual task for
both groups and volumes, we observed that both the 3-mL and 5-mL volumes showed a
statistically significant difference for the PD group, with no difference in the HC
group. There was significant difference between scores for the 3-mL and 5-mL volumes
for either task in the two groups ([Table 2 ]).
Table 2
Comparison between the groups and tasks, and results of the Boston Residue and Clearance
Scale for the 3-mL and 5-mL volumes
Variables
Parkinson disease patients
Healthy controls
p -value*
(n = 19)
(n = 19)
Median (25–75%)
Median (25–75%)
3 mL
Single swallow
2 (1–2)
0 (0–1)
< 0.001
Dual-task
4 (2-6)
0 (01)
< 0.001
p -value**
0.014
0.480
5 mL
Single swallow
2 (1–4)
0 (0–1)
< 0.001
Dual-task
4 (2–6)
1 (0–2)
< 0.001
p -value**
0.025
0.366
Notes:*Comparison between groups using the Mann-Whitney test; ** comparison between
tasks for each group using the Wilcoxon test.
[Table 3 ] evaluates the correlation between the BRACS score and the H&Y, MoCA, and MMSE scores.
No significant correlation was found between the BRACS scores and the degree of severity
of PD as evaluated by the H&Y, MMSE, MoCA, and DD scores ([Table 3 ]).
Table 3
Correlations of variables with the Boston Residue and Clearance Scale by group using
the Spearman correlation coefficient (rs )
Parkinson disease patients
Healthy controls
Hoehn &Yahr Scale
Montreal Cognitive Assessment
Mini Mental State Examination
Disease Duration (yr)
Montreal Cognitive Assessment
Mini Mental State Examination
3 mL
Single task
rs = 0.029
rs = 0.117
rs = 0.090
rs = 0.139
rs = -0.064
rs = 0.013
(p = 0.908)
(p = 0.632)
(p = 0.715)
(p = 0.581)
(p = 0.796)
(p = 0.957)
Dual task
rs = -0.208
rs = -0.369
rs = 0.308
rs = -0.104
rs = 0.057
rs = 0.109
(p = 0.392)
(p = 0.120)
(p = 0.199)
(p = 0.681)
(p = 0.817)
(p = 0.658)
5 mL
Single task
rs = 0.096
rs = -0.054
rs = 0.033
rs = 0.166
rs = -0.032
rs = 0.039
(p = 0.695)
(p = 0.826)
(p = 0.892)
(p = 0.510)
(p = 0.896)
(p = 0.874)
Dual task
rs = 0.241
rs = -0.027
rs = 0.230
rs = 0.067
rs = -0.058
rs = -0.037
(p = 0.320)
(p = 0.913)
(p = 0.345)
(p = 0.792)
(p = 0.814)
(p = 0.882)
[Fig. 1 ] shows a comparison of the variations in the BRACS, that is, the difference in the
variation to describe differences between the dual-task and isolated-swallowing tests
for each volume. There was greater variability in the results of the BRACS scores
in the PD group when compared with the HC group. The differences were only significant
for the 3-mL volume (p = 0.012). For the 5-mL volume, the difference was borderline (p = 0.053).
Fig. 1 Comparison of the results of variations of the BRACS for the dual task when compared
with swallowing for each study group.
[Fig. 2 ] shows the correlation between the performance on the MoCA and the variation in the
3-mL volume results. There was an inverse, significant association between the results
of the MoCA with the change in BRACS scale between the dual task and isolated task
only the in PD group (rs = -0.480; p = 0.038). The patients who had lower scores on the MoCA were those with greater variation
in swallowing during the two tasks. In the control group, the association was not
significant (rs = 0.093; p = 0.704). There was no significant correlation between variations in the BRACS score
and other clinical variables (p > 0.05).
Fig. 2 Association between the differences in MoCA results and BRACS scores in the comparison
of the 3-mL dual-task and isolated-swallowing tests.
Discussion
When patients with PD simultaneously performed a motor task during swallowing, the
swallowing parameters, as assessed by the FEES, decreased for both the 3-mL and 5 -mL
swallow test, that is, motor activity became more important than swallowing, which
caused an interference in the normal swallowing physiology. This interference was
not observed in the control group.
The change in the swallowing symptom residue among PD patients reveals an effect on
swallowing safety regarding the increased motor demand/cognitive ability required
to conduct the motor task. These findings are consistent with those in the literature,
indicating that motor tasks, such as walking, may be affected by external cognition
competition or motor tasks.[16 ]
In a previous study,[26 ] finger tapping and swallowing were used as a paradigm to compare the right and left
hands during an intake of 300 mL of liquid barium, which was swallowed by healthy
subjects and evaluated by videofluoroscopy. The aim of the study was to analyze the
differences between the right and left hands to assess the lateralization of swallowing
in the cortex by measuring the speed of manual movement. Finger tapping may set the
pace by influencing the swallowing pattern. Despite methodological differences from
our study, the task performance also changed in the dual-task condition with an increasing
score, suggesting a higher demand for the combined task. A statistically significant
increase in the BRACS score under the 3-mL and 5-mL volume conditions was evident
in the PD group. There are no published studies using the FEES and motor tasks for
comparison; however, the results of the study by Troche et al[18 ] were consistent that swallowing is influenced by dual-task condition.
The FEES provides information about the anatomical and physiological patterns of residue
problems. Visualization is concentrated toward the pharyngeal stage of swallowing;
therefore, it is sensitive in detecting the amount of residue.[22 ] The presence of residue in the laryngopharyngeal segment indicated significant results
during dual-task swallowing, and was one of the main factors analyzed in the present
study. This may contribute to decreased patient safety due to an increased risk of
aspiration as a result of accumulation of secretions in different parts of the respiratory
tract. Previous studies[4 ]
[27 ] with PD patients demonstrated that residue in the valleculae or upper esophageal
sphincter and fractionation of swallowing are associated with penetration/aspiration.
As shown in [Table 2 ], the present study demonstrated a statistically significant difference between the
performance of the single task (isolated swallowing) and of the dual task (swallowing + manual
movement), despite the lack of existing literature using the same functional paradigm
for swallowing. In the study by Pinto et al,[20 ] the competition between manual tasks and speech in PD patients resulted in a loss
of the first task because of the second. For healthy adults, a combination of motor
movements can be performed simultaneously, but this is not true for patients with
PD.
The present study revealed that PD patients had impairments in cognitive function
according to the MoCA and MMSE scores when compared with the HCs. Data from the BRACS
showed that patients, even without any swallowing complaints, presented with impaired
food safety as observed by the increase in the score. A limitation of the BRACS is
the absence of a standard to determine a cut-off point for food safety. This was not
the objective of the present work, but we were able to identify a variation in food
safety in the dual-task test. Subsequent studies or meta-analysis data are needed
to determine these standards for future analysis.
It has been observed that PD patients experience great difficulty with automatic movements
beginning with the early stages of the disease, and these difficulties worsen when
combined with other movements. These observations suggest that normal movement patterns
are not lost, but are interrupted by competing motor and cognitive tasks.[28 ] Swallowing can be considered a skill with conscious and automatic components directly
related to each stage of the physiology. In the dual-task assessment, simultaneous
motor movements caused dysfunction in swallowing physiology.
However, one limitation of the present study is the difficulty in establishing cut-off
points for food safety with the BRACS. Second, both the volume and consistency of
the bolus used were lower than the corresponding daily food consumption of the patients,
which reduced the amount of residue found during the FESS assessment. This suggests
that increasing the volume may involve safety risks, especially for patients with
PD. Therefore, the volume and consistency were selected to determine the physiology
of swallowing without compromising the safety of the testing.
The present study describes novel research regarding concurrent tasks on swallow physiology,
but has limitations that should be considered when interpreting the results. The high
variability in the sample may have limited the degree to which subtle changes could
be statistically assessed. Replication of this study with a larger sample, comparing
different stages, or a more homogeneous sample based on disease stage is necessary.
Despite the aforementioned limitations, we believe that the elaborate experimental
design of the study was appropriate for the dual-task design, to safe and efficient
swallowing and FEES results.
The use of FEES for research is more recent than the video fluoroscopic swallowing
exam. The FEES is now a gold standard to evaluate, and it is validated by the use
of scales that enable diagnostic analysis of dysphagia as well as a comparative analysis.[14 ]
The analysis of the cognitive performance of patients and controls via competitive
tasks showed that there was an inverse correlation between the MoCA scores and the
scores of the dual and individual tasks in the PD group, demonstrating that PD patients
did not perform as well according to the MoCA, and that they had a decreased performance
in the 3-mL volume test ([Fig. 2 ]). This was not the case for the 5-mL volume test, which can be attributed to a habituation
and learning phenomenon following task presentation. The lack of correlation between
the results of the cognitive tests is probably related to the nature of the tasks
involved in the testing. The act of swallowing does not occur in isolation in daily
life. However, limited information is available regarding interference of the external
environment and concomitant motor tasks during swallowing. Distractions, such as cognitive
and motor interference, can impair swallowing, which increases the complexity of the
compensation reactions performed by the patients. However, situations that arise during
evaluation and therapy occur in isolated and controlled environments with no external
interference, which enables the patients to keep their focus on swallowing. Thus,
this controlled environment may not reproduce the real situations of daily feeding
conditions, which are worse than those found in the evaluation and therapy. Therefore,
further studies are needed to understand the interference of motor and cognitive tasks
in concomitant swallowing to elucidate the environmental changes that may occur routinely
in patients with PD.
Conclusion
The participants in this PD study demonstrated worse swallowing safety in the dual-task
versus single-task conditions. These data may reveal the inability of PD patients
to coordinate the performance of concomitant tasks such as swallowing and manual movement.
This finding was not observed in the control group, which suggests the potential interference
of motor and cognitive competition in dual-task functions.
