Dysphagia (2008) 23:136145

DOI 10.1007/s00455-007-9113-4

ORIGINAL ARTICLE

The Coordination of Breathing and Swallowing in Parkinsons

Disease
Roxann Diez Gross Charles W. Atwood Jr.
Sheryl B. Ross Kimberly A. Eichhorn
Joan W. Olszewski Patrick J. Doyle

Published online: 20 November 2007

Springer Science+Business Media, LLC 2007

Abstract Multiple investigations have determined that

healthy adults swallow most often during exhalation and
that exhalation regularly follows the swallow, even when a
swallow occurs during inhalation. We hypothesized that
persons with idiopathic Parkinsons disease would demonstrate impaired breathing and swallowing coordination
during spontaneous eating. Twenty-five healthy volunteers
and 25 Parkinsons disease patients spontaneously swallowed calibrated pudding and cookie portions while
simultaneous nasal airflow and respiratory inductance
plethysmography were used to track spontaneous breathing. Surface EMG was used to record the timing of each
swallow within the respiratory cycle. When compared to
the healthy control group, those with Parkinsons disease

swallowed significantly more often during inhalation and at

low tidal volumes. The Parkinsons participants also
exhibited significantly more postswallow inhalation for
both consistencies. Only the healthy subjects exhibited
significantly longer deglutitive apnea when swallows that
occurred during inhalation were compared with those that
occurred during exhalation. The high incidence of oropharyngeal dysphagia and risk of aspiration pneumonia
found in Parkinsons disease patients may be partially
attributable to impaired coordination of breathing and
swallowing.

This work was performed at the VA Pittsburgh Healthcare System,

University Drive location, and was funded by the Department of
Veterans Affairs Research and Rehabilitation Merit Review
Program.

The prevalence of idiopathic Parkinsons disease (IPD) rises

sharply with age, and a three- to fourfold increase in disease
rate within the United States is expected to occur over the
next ten years [1]. Aspiration pneumonia is a major cause of
morbidity and mortality in persons with Parkinsons disease,
signifying that prandial aspiration should be a major concern
[26]. Accordingly, videofluoroscopic examination of
swallowing function has revealed abnormal findings in up to
100% of those with IPD even though those with IPD are often
unaware of any swallowing problems [79].
Dysphagia can develop at any point during the disease.
Whereas dysphagia is prevalent in long-standing IPD,
swallowing impairments can occur early in the disease as
well. Indeed, some have suggested that subclinical dysphagia can be one of the initial symptoms of IPD [9, 10].
IPD motor symptoms worsen over time, but disease
severity cannot reliably foretell the presence nor degree of
dysphagic impairment for those with IPD [11]. Two

R. D. Gross (&)
S. B. Ross

Division of Otolaryngology, University of Pittsburgh,
Eye & Ear Institute, Suite 500,
200 Lothrop Street, Pittsburgh, Pennsylvania 15213, USA
e-mail: Grossrd@upmc.edu
C. W. Atwood Jr.
K. A. Eichhorn
VA Pittsburgh Healthcare System, University Drive C,
Pittsburgh, Pennsylvania 15240, USA
J. W. Olszewski
Henry Ford Hospital, 2799 W. Grand Blvd., Detroit,
Michigan 48202, USA
P. J. Doyle
VA Pittsburgh Healthcare System, Highland Drive, Pittsburgh,
Pennsylvania 15240, USA

123

Keywords Parkinsons disease
Oropharyngeal

dysphagia
Swallowing
Respiratory control

Deglutition
Deglutition disorders
Subglottic air pressure

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

investigations that used fluoroscopy to assess swallowing

function with liquids and solids did not determine correlation between Hoehn & Yahr rating and dysphagic
findings [11, 12]. Similar findings have been reported with
clinical swallowing evaluations using water challenges
[13]. For example, Clark et al. [14] used a water challenge
and found a decline in swallowing speed that correlated
with Hoehn & Yahr scores, but they reported a lack of
correlation between disease duration and their dysphagia
measures.
Oropharyngeal dysphagia in IPD is inconsistently
responsive to pharmacologic therapy. Several investigators
have fluoroscopically examined swallowing function in the
same group of IPD patients both with and without dopaminergic medication and found that swallowing
abnormalities usually persist after the administration of the
drug, even when the dose is increased [13, 1517]. Likewise, surgical interventions such as pallidotomy,
thalamotomy, gamma knife, and deep brain stimulation
have not been shown to have consistent or positive effects
on swallowing function [18, 19]. In fact, worsening dysphagia is often cited as a complication of surgical
intervention [20, 21]. In summary, the pathophysiology of
dysphagia in IPD has not been fully explained.
The effect of levodopa and dopamine agonists on
breathing patterns and certain measures of pulmonary
function also remains controversial. Some investigators
have concluded that levodopa can induce respiratory dyskinesia [22, 23], while others report that anti-Parkinsons
drug therapy can partially alleviate restrictive breathing
patterns [24, 25]. Consistent with dysphagia, individuals
with IPD are often unaware of respiratory impairment and
declines in pulmonary function frequently go unrecognized
until serious complications arise [26, 27]. Consequently,
impaired pulmonary function in IPD not only has the
potential to lower tolerance of aspiration, it also has the
propensity to disrupt proper coordination between breathing and swallowing. The significance of proper
coordination between respiration and deglutition is
increasingly recognized as important to swallowing safety.
Many investigations have shown that healthy adults
exhibit a predominant exhale-swallow-exhale pattern to
coordinate breathing and swallowing [2831]. Exhalation
has been found to almost invariably follow each swallow,
even should one occur during the inhalation phase [32]. A
strong preference for timing swallows at early to midexhalation has also been reported [28, 31, 33]. Deviation
from the normal pattern, particularly postswallow inhalation, can place individuals at risk for aspiration [34].
Pinnington et al. [35] studied the coordination of breathing
and swallowing in IPD subjects using a specialized noninvasive technique. They showed that when given a thin
liquid from a spoon, the IPD subjects inhaled after

137

swallowing significantly more than control subjects. To

build upon their findings and gain further insight into the
problem, we sought to additionally characterize swallowing-related respiratory patterns in patients with IPD.
Therefore, the purpose of our study was to noninvasively
measure respiratory characteristics surrounding swallows
of IPD participants and controls. We hypothesized that
persons with IPD would show a disorganization of the
normal coordination of breathing and swallowing while
spontaneously eating semisolids and solids.

Methods
The study was a prospective repeated-measures design.
Two groups were studied: one with idiopathic Parkinsons
disease and a healthy, similarly aged control group. Using
historical data on the proportions of swallows occurring
during exhalation for normal and neurologically impaired
participants [36] (an alpha level of 0.05, and power of 0.8),
it was determined that 25 subjects per group would be
required to detect a moderate effect. This study was
approved by the VA Pittsburgh Health Systems Institutional Review Board and all subjects gave written consent
prior to screening and participation.
The mean age of the 25 volunteers with IPD was 71
years (range = 5384, SD = 9.86). All participants were
male because they were recruited from the largely male
veteran population. Idiopathic IPD was diagnosed and
rated as stage 2 or 3 on the Hoehn & Yahr disability scale
by a board-certified neurologist. The average Hoehn
&Yahr rating for the group was 2.4. None of the participants had a previous history of other neurologic disease,
stroke, head and neck cancer, lung cancer, or chronic
obstructive pulmonary disease. In addition, each had to
receive the following individual scores on the Unified
Parkinson Disease Rating Scale (UPDRS): Intellectual
Impairment score of 0 (normal), Thought Disorder score of
2 or less, Depression score of 2 or less, Motivation/Initiative score of 3 or less, Speech score of 2 or less, Salivation
score of 2 or less, Swallowing score of 3 or less. Table 1
shows the number of participants that received each
acceptable score. Oropharyngeal swallowing function was
not instrumentally assessed, but at the time of this study all
participants were receiving 100% of their nutrition and
hydration orally and all stated that semisolids like pudding
and soft solids such as sugar cookies were part of their
daily diet. In addition, the delayed/immediate recall ratio
on the Story Retelling-Immediate/Story RetellingDelayed
subtests of the Arizona Battery for Communicative Disorders of Dementia was used to rule out dementia [37].
This ratio, which compares the amount of information
recalled in an immediate condition compared to the amount

123

138

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

Table 1 UPDRS ratings and number of subjects who received each

rating
UPDRS scores

No.
subjects

Intellectual impairment
0 (normal)
Thought disorder
0 (normal)

25
15

1 (vivid dreaming)

2 (benign hallucinations with insight retained)

Depression
0 (normal)
1 (periods of sadness/guilt greater than normal)

24
1

Motivation/Initiative
0 (normal)

20

1 (less assertive than usual; more passive)

2 (loss of initiative or disinterest in elective activities)

Speech
0 (normal)

14

1 (mildly affected; no difficulty being understood)

2 (moderately affected; sometimes asked

to repeat statements)

Salivation
0 (normal)
1 (slight but definite excess of saliva in mouth;
may have nighttime drooling)
2 (moderately excessive saliva;
may have minimal drooling)
Swallowing
0 (normal)
1 (rare choking)

9
12
4

20
2

2 (occasional choking)

3 (Requires soft food)

of information recalled approximately 60 minutes later

(delayed) is multiplied by 100 to yield the percentage
remembered. Bayles et al. [38] showed that normal elderly
subjects (mean age = 70, SD = 7.25) will forget on average
only *4% of the information that they immediately
recalled, while mild dementia patients will forget *98%.
All individuals enrolled had a delayed/immediate recall
ratio that was greater than 95%.
The average age of the 25 normal subjects was 64 years
(range = 5181, SD = 9). There were 12 males and 13
females. The controls denied any history of dysphagia,
neurologic disease, stroke, head and neck cancer, lung
cancer, or chronic obstructive pulmonary disease. Appendix A contains the questionnaire that was used to question
potential subjects. To assure that the healthy group did not
have any pulmonary dysfunction, spirometry was used to
exclude individuals with an FEV1/FEV \70%. Individuals
whose delayed/immediate recall ratio was below 95% were

123

also excluded from participation. No one was excluded

from participation in either group because of gender or
religious or ethnic background.
The KayPentax Swallowing Station with Swallowing
Signals Lab (Lincoln Park, NJ) was used to provide a timelocked display and recording of natural breathing and swallowing behaviors. Respiratory measures were obtained using
two measurement techniques that in combination have been
shown to be optimal for deglutition studies because they do
not require any apparatus involving a facemask [39].
Respiratory inductance plethysmography (Respitrace,
Ambulatory Monitoring Inc., Ardsley, NY) was used to track
changes in cross-sectional area of the rib cage and abdomen,
allowing for tracking and determination of inhalation and
exhalation using direction of motion. In addition, a nasal
cannula that connected to a transducer in the Swallowing
Signals Lab was used to determine the direction and duration
of nasal airflow. To detect and record each swallow event,
surface electromyographic electrodes (SEMG) were affixed
under the chin behind the mental symphysis (submental
placement). The submental muscle group includes the
mylohyoid, anterior belly of the digastric, and geniohyoid
and has been shown to be a valid and reliable indicator of the
pharyngeal swallow [40]. The combined signals of the
SEMG peak that is associated with the activation of swallowing muscles and the interruption of the nasal airflow
signal that is consistent with deglutitive apnea provided a
robust indicator of the point in time within the breathing cycle
that each swallow occurred. Figure 1 shows an example of
raw data. No medication adjustments were made and all of
the recordings of IPD participants were taken during on
periods. None of the study volunteers in either group had an
active respiratory infection at the time of data collection.
After placement of the Respitrace, nasal cannula, and
SEMG, participants were seated at a table while they selffed and spontaneously swallowed ten 5-ml semisolid
boluses (pudding) that were premeasured onto individual
teaspoons (1/2 serving). Participants also chewed and
swallowed naturally (without prompting) nine 2.5-g solid
portions that were laid out on a small plate ( 3 vanilla wafer
cookies). Nineteen bolus swallows per participant were
obtained. Participants were instructed to eat normally
and to choose whatever you would like in whatever order
you prefer. The instructions resulted in spontaneous randomization of time intervals within and between
consistencies because each subject demonstrated a unique
pattern while eating.

Data Analysis
Blinding procedures were used during the determination of
respiratory characteristics surrounding each swallow.

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

Interrater and intrarater reliability measurements were also

made under blinded conditions. Swallows that could not be
identified easily, food boluses that were not swallowed in a
single attempt, or swallows with inconsistency between
nasal airflow and plethysmography signals were not used in
the final analysis. A total of 230 of 250 pudding swallows
from the control group and 235 of 250 from the Parkinsons
group were analyzed. A total of 214 of 225 cookie swallows
were suitable for analysis from the healthy control group
and 211 of 225 from the Parkinsons group. Each swallow
was noted by the nearly simultaneous appearance of deglutitive apnea where nasal airflow ceases while the airway is
closed and a peak in the rectified and integrated SEMG
appears when swallowing muscles are activated. These
combined signals were also used to distinguish periods of
breath-holding and mouth-breathing from deglutitive apnea
because only bolus swallows gave a time-linked apnea/
SEMG signal. Respiratory phase in which the swallow
occurred and postswallow respiratory phase were determined using the combined nasal airflow and
plethysmographic signals. When mouth breathing resulted
in a temporary loss of nasal airflow, the signal from plethysmography was used to determine respiratory phase so
long as there had been good correlation between nasal and
plethysmography traces. Because swallows that occur at or
near end-inhalation are associated with higher tidal volumes
relative to swallows that occur at or near end-exhalation,
measurements of high vs. low tidal volume were also made.
To estimate tidal volume at the time of the swallow (high

139

vs. low), the duration of the exhalation or the inhalation

phase was determined in milliseconds using the Swallowing
Signals Lab software and then divided into four equal
quadrants. Only the first and last quadrants were used to
classify swallows into early or late inhalation or exhalation.
The duration of deglutitive apnea (DDA) was taken as the
length of time that the nasal signal returned to baseline (zero
flow), indicating airway closure associated with swallowing
[41]. Overall intra- and interrater reliability was acceptable
as calculated by intraclass correlations ranging from 0.69 to
0.71 for all measurements.

Results
In the control group, the proportion of swallows of both
consistencies that occurred during exhalation and were
followed by exhalation was consistent with previous
reports [30, 42]. Logistic regression analysis showed that,
when compared to the healthy controls, the IPD group
swallowed significantly more often during inhalation,
regardless of whether a semisolid (pudding) or solid
(cookie) was consumed. The IPD participants also exhibited significantly more postswallow inhalation for both
consistencies. In addition, those in the IPD group swallowed both consistencies at low tidal volume significantly
more frequently than those in the control group. Tables 24
are the statistical tables from the analysis and Fig. 2 is a
graphic display of the data.

Fig. 1 Example of raw data.

The vertical line running
through the boxes shows the
time point at the beginning of
deglutitive apnea. The top box
is the signal from the nasal
cannula. The box below the
cannula shows the
plethysmographic signal from
the band that was around the
chest. The third box from the
top shows a combination of
chest and abdomen band signals
that represent tidal volume
changes. The box at the bottom
shows the submental EMG
signal

123

140

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

A significant difference between inhalation vs. exhalation

of DDA within the IPD group was not found. However,
within the healthy group, DDA was significantly longer for
swallows occurring during inhalation when compared to
swallows that were timed with exhalation. Tables 5 and 6
are statistical tables and Fig. 3 is a graphical representation
of the data.

Table 2 Swallow during inhalation

Group

Consistency Event/total Odds ratio 95% CI

Healthy Cookie

4/214

IPD

29/211

Cookie

Healthy Pudding

22/230

IPD

39/235

Pudding

p Value

8.37

8.9, 24.2

0.0001

1.9

1.08, 3.20 0.0264

Table 3 Postswallow inhalation

Group

Consistency Event/total Odds ratio 95% CI

Healthy Cookie

20/214

IPD

52/210

Cookie

Healthy Pudding

17/230

IPD

60/235

Pudding

Discussion

p Value

3.2

1.83, 5.57 \0.0001

4.30

2.42, 7.63 \0.0001

The findings of this investigation indicate that persons with

IPD may be more likely to swallow at abnormal times
within the respiratory cycle, such as during inhalation or at
low tidal volume. Individuals with IPD are also more likely
to inhale after swallowing, even when swallowing during
the exhalatory phase. The lack of proper coordination of
breathing and swallowing may be an important underlying
factor for dysphagia and place patients with IPD at
increased risk for aspiration. For example, Morton et al.
[34] studied neurologically impaired children under fluoroscopy and showed that inhalation after the swallow
resulted in aspiration, with chaotic respiration being
highly associated with aspiration. Recognizing that respiratory conditions surrounding the swallow are likely to
affect performance, it must also be determined if aspiration
is purely a mechanical phenomenon where pharyngeal
residue enters the airway via negative airflow (inhalation),
or if there is a basic physiologic mechanism that is operating as well.
The presence of laryngeal subglottic mechanoreceptors
has been confirmed [43, 44] and recent investigations
demonstrated that they are likely to have a role in swallowing motor control [4548]. It has been suggested that a

Table 4 Swallow at low tidal volume

Group

Consistency Event/total Odds ratio 95% CI

Healthy Cookie
IPD
Cookie

17/214
54/211

Healthy Pudding

16/230

IPD

54/235

Pudding

p Value

2.4

1.43, 3.96 0.0008

4.0

2.21, 7.21 \0.0001

The duration of airway closure (deglutitive apnea) was

also measured. The Wilcoxon 2-sample test determined
that the difference between the overall DDA between the
two groups was not significant. Because the focus of this
experiment was on the timing of swallows within the
respiratory cycle, comparisons of DDA for swallows
occurring during inhalation vs. exhalation were also made.
Fig. 2 Percentage of swallows
occurring at times other than the
preferred pattern of exhaleswallow-exhale: healthy
controls vs. Parkinsons disease

Timing of spontaneous swallows within breathing cycle

Heathy controls vs. Parkinson's disease
30
Healthy control
Parkinson's disease

Percentage of swallow

25

20

15

10

0
Cookie

Pudding

Swallow during inhalation

123

Cookie

Pudding

Inhalation after swallow

Cookie

Pudding

Low tidal volume

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

141

Table 5 Duration of deglutitive apnea in milliseconds during exhalation vs. inhalation

Group

Statistic

Exhale DDA

Inhale DDA

p Value

Healthy

347

26

0.025

Mean, SD

649, 133

887, 274

Median

670

801

Q1, Q3

609, 748

744, 921

Min, Max

377, 1357

576, 1744

Table 6 Duration of deglutitive apnea in milliseconds during exhalation vs. inhalation

Group

Statistic

Exhale DDA

Inhale DDA

p Value

IPD

272

49

0.308

Mean, SD

643, 133

665, 182

Median

624

609

Q1, Q3

558, 692

545, 705

Min, Max

409, 1300

417, 1325

higher lung volume at the time of the swallow will result in

greater subglottic air pressure during the swallow (deglutitive subglottic pressure or DPsub) [45, 49]. Perhaps the
larynx should be viewed as more than a simple device that
protects the airway, but also as an organ that has neuroregulatory capabilities related to swallowing function.
Thus, positive stimulation of subglottic mechanoreceptors
by exhalatory flow before the swallow and sufficient
positive air pressure during the swallow could optimize
swallowing function. Once stimulated, the pressurized
larynx may signal feedback mechanisms related to swallowing pharyngeal motor control that are necessary to
enable safe and efficient bolus passage. For example, the
pressurized larynx may signal to the brainstem central
pattern generator for swallowing that it is well pressurized
and, therefore, the swallow will continue with maximum
Fig. 3 Comparison between the
duration of swallowing apnea
for swallows occurring during
exhalation vs. inhalation

speed and force (i.e., greatest efficiency). Alternatively,

should subglottic receptors indicate an inadequate level of
pressurization (low lung volume or negative airflow such as
during inhalation), the motor program may be altered so as
to reduce the muscle force generated within the pharynx
(i.e., less efficiency).
Greater amounts of pharyngeal residue and aspiration
have been observed in the same patients with open tracheostomy tubes where subglottic air pressure is absent,
but not when the tube is occluded [47, 48, 5052]. However, the effect has not been observed in all tracheostomy
subjects [53, 54]. A possible explanation for why simple
occlusion of the tube does not consistently improve swallowing function may lie within coordination of breathing
and swallowing. Thus, even when the tracheostomy tube is
occluded, should a swallow occur at low tidal volume,
DPsub will be insufficient and potential benefits will not
occur [49]. In addition, inhalation after the swallow may
also increase aspiration rate regardless of occlusion status.
Any or all of the respiratory characteristics of IPD
patients can potentially disrupt the coordination of the
respiratory cycle with swallowing. Pulmonary function
testing of patients with IPD has revealed that subclinical
respiratory impairment is common [26, 27, 55, 56]. Respiratory insufficiency is most likely due to the threefold
nature of the diseases progressive motor dysfunction: (1)
postural abnormalities that restrict chest and abdominal
movement [57], (2) low chest wall compliance secondary to
muscle rigidity [58], and (3) lack of coordination between
agonist and antagonist respiratory muscle groups [26].
Disruptions in pulmonary mechanics may induce swallows
that occur at inopportune times within the respiratory cycle.
A high percentage of patients with Parkinsons disease
also demonstrate voice disorders that are characterized by
reduced loudness and breathiness. These subjective observations are often indicative of vocal fold bowing and
glottal incompetence [5961]. The Lee Silverman Voice
Apnea duration of swallows occuring during exhalation vs. inhalation

900
Inhalation
800

Median duration in Milliseconds

700

Exhalation
Exhalation

Inhalation

600
500
400
300
200
100
0
Healthy

Parkinson's

123

142

Therapy (LSVT) [62, 63] is an established treatment to

improve vocal intensity in persons with IPD. Although a
specific treatment for dysphagia in IPD patients has not
been validated [64, 65], LSVT has been suggested as an
effective swallowing therapy. Prompted by patients
reports of better swallowing function coinciding with
increased vocal volume, a preliminary study that used eight
patients who served as their own controls was completed
by Sharkawi et al. [66]. Under fluoroscopy, they noted
improved oropharyngeal swallowing efficiency following
LSVT. The authors postulated that an overflow of effort
or improved function within the brains insular cortex
could have been responsible for the swallowing improvements. Additional plausible explanations are that greater
subglottal pressures were generated not just during phonation [67] but also while swallowing and/or that improved
breathing and swallowing coordination resulted from the
therapy.
As a secondary analysis, DDA was compared between
swallows that occurred during inhalation and exhalation.
Only the healthy subjects made adjustments between the
two respiratory conditions. This finding indicates that the
healthy participants may have employed a compensatory
strategy. Examples of compensation might be prolonged
airway protection during inhalation swallows, or possibly
prolonging DDA to allow additional time for adequate
DPsub to build up. Such compensation appeared to be
absent within the Parkinsons disease group (Fig. 2).
Studies that have compared swallowing physiology under
different respiratory conditions reported significant differences in durational measures when swallows that occurred
at low lung volume were compared with high-lung-volume
swallows, or when open tracheostomy tube vs. occluded
tracheostomy tube comparisons were made [45, 46, 54].
Additional support for our suggested interpretation is provided by a Kijima et al. [68] who studied young healthy
subjects who swallowed with and without respiratory
loads. The investigators found that the coordination of
breathing and swallowing moved away from normal
exhale-swallow-exhale patterning with different respiratory
loads but the DDA was not altered. Relevant to our current
study is that they observed that laryngeal irritation (i.e.,
coughing) occurred when swallows were timed at the
exhalation-to-inhalation (E-I) transition that was brought
on by elastic loading. Swallows that occur at E-I transition
would be associated with a lower tidal volume and be
expected to have a lower DPsub than swallows that are
timed with inhalation-to-exhalation (I-E) or early to midexhalation. The lack of a durational change in DDA and
subsequent coughing may be indicative of a failure to make
compensatory adjustments for swallowing at times other
than the preferred. Thus, the liquid entered the airway and
caused the subjects to cough.

123

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

As stated previously, Pinnington et al. [35] studied the

breathing and swallowing patterns of IPD participants (n
= 12) using liquids. In their IPD group, 83% of liquid
swallows occurred during exhalation, but this did not
represent a significant difference from their control group
where 88% of the swallows interrupted exhalation.
Interestingly, the results of our study also found that 83%
of IPD swallows of pudding occurred during exhalation,
yet this was significantly lower than that of our control
group where 90% of pudding swallows occurred during
exhalation. Possible explanations for this difference are
that we had an adequate sample size to reach significance
(n = 25), or that the solid and semisolids used in our
experiment were more likely to disrupt breathing and
swallowing patterns. In both studies, the percentage of
swallows that were followed by inhalation was significantly higher than the control group (20%, p = 0.03 in
Pinnington et al., and 26%, p 0.0001 in ours).

Limitations
The primary limitation of this study is that we relied on
chart review and the IPD volunteers perception of their
swallowing and pulmonary function. Therefore, we cannot say with certainty if any of the IPD participants had
subclinical dysphagia or pulmonary disease. For this
initial study we wanted to first determine if impaired
breathing/swallowing coordination was present in a typical sample of clinic patients. Another potential criticism
is that we did not quantify tidal breathing using a nasal
mask. However, the main objective was to create as
natural an environment as possible so that we could
observe spontaneous behaviors and a nasal mask could
influence spontaneity.

Conclusion
Accurate coordination between breathing and swallowing
could be the key to swallowing safety in IPD because
sufficient subglottic air pressure is easiest to generate at
higher tidal volumes. Furthermore, exhalatory airflow after
the swallow can serve as an airway-clearing mechanism if
any material entered the airway while swallowing [31].
Impaired coordination between breathing and swallowing
in IPD patients is likely to have a negative effect on
swallowing performance and can help to explain the high
prevalence of dysphagia that occurs at any point during the
disease, regardless of severity. This rationale can also
partially explain why anti-Parkinson drugs do not consistently improve swallowing function or prevent the
development of oropharyngeal dysphagia.

R. D. Gross et al.: Breathing/Swallowing in Parkinsons Disease

143

Appendix A
Screening Questionnaire for Interested Individuals

Subject ID_________

What happens when you drink thin liquids such as water, coffee, tea or juice?
What happens when you eat solid food?
Are there any foods that you avoid? If so, why?
Do you have any difficulty swallowing?
Have you had any difficulty swallowing in the last 6 months other than
a sore throat?
Have you ever been diagnosed with a stroke or a ministroke?
Have you ever thought that you had stroke or a ministroke?
Have you ever had a serious head injury that required a hospital stay?
Have you ever been diagnosed with a progressive neurological disease
such as Parkinsons disease, multiple sclerosis (MS), ALS (Lou Gherigs
disease) or myasthenia gravis?
Do you think that you have a progressive neurological disease such as
Parkinsons disease, multiple sclerosis (MS), ALS (Lou Gherigs disease)
or myasthenia gravis?
Have you ever been diagnosed with a muscle disease such as polymyositis,
sarcoidosis, myotonic dystrophy, or oculopharyngeal dystrophy?
Do you think that you might have a muscle disease?
Have you ever been diagnosed with oral or pharyngeal (throat) cancer?
Have you ever had an oral or throat tumor removed?
Have you ever had any surgery to your tongue or to the inside or outside
of your neck?
Have you ever been diagnosed with chronic obstructive pulmonary disease
(COPD) or emphysema?
Do you think that you might have chronic obstructive pulmonary disease
(COPD) or emphysema?
Do you have any difficulty breathing?

Yes

No

Yes
Yes
Yes
Yes

No
No
No
No

Yes

No

Yes

No

Yes
Yes
Yes
Yes

No
No
No
No

Yes

No

Yes

No

Yes
Yes

No
No

References
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1902.
Roxann Diez Gross PhD
Charles W. Atwood Jr. MD
Sheryl B. Ross MA
Kimberly A. Eichhorn MS
Joan W. Olszewski MA
Patrick J. Doyle PhD

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