The Coordination of Breathing and Swallowing in Parkinson’s

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O R I G I N A L A R T I C L E

The Coordination of Breathing and Swallowing in Parkinson’sDisease

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 andthat exhalation regularly follows the swallow, even when a

swallow occurs during inhalation. We hypothesized that

persons with idiopathic Parkinson’s disease would dem-

onstrate impaired breathing and swallowing coordination

during spontaneous eating. Twenty-five healthy volunteers

and 25 Parkinson’s disease patients spontaneously swal-

lowed calibrated pudding and cookie portions while

simultaneous nasal airflow and respiratory inductance

plethysmography were used to track spontaneous breath-

ing. Surface EMG was used to record the timing of each

swallow within the respiratory cycle. When compared to

the healthy control group, those with Parkinson’s disease

swallowed significantly more often during inhalation and at

low tidal volumes. The Parkinson’s participants alsoexhibited 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 oro-

pharyngeal dysphagia and risk of aspiration pneumonia

found in Parkinson’s disease patients may be partially

attributable to impaired coordination of breathing and

swallowing.

Keywords Parkinson’s disease Oropharyngeal

dysphagia

Swallowing

Respiratory control

Deglutition Deglutition disorders Subglottic air pressure

The prevalence of idiopathic Parkinson’s 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 Parkinson’s disease,

signifying that prandial aspiration should be a major concern

[2–6]. 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 [7–9].

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 dys-

phagia 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

This work was performed at the VA Pittsburgh Healthcare System,

University Drive location, and was funded by the Department of

Veteran’s Affairs Research and Rehabilitation Merit Review

Program.

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: [email protected]

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

1 3

Dysphagia (2008) 23:136–145

DOI 10.1007/s00455-007-9113-4



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 = 51–81, 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. Appen-

dix 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

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 time-

locked display and recording of natural breathing and swal-

lowing behaviors. Respiratory measures were obtained using

two measurement techniques that in combination have beenshown to be optimal for deglutition studies because they do

not require any apparatus involving a facemask [39].

Respiratory inductance plethysmography (Respitrace,

Ambulatory MonitoringInc., 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 (submentalplacement). 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 swal-

lowing muscles and the interruption of the nasal airflow

signal that is consistent with deglutitive apnea provided a

robustindicator of thepointin time withinthe breathingcycle

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 self-

fed 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 ran-

domization 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.

Table 1 UPDRS ratings and number of subjects who received each

rating

UPDRS scores No.

subjects

Intellectual impairment

0 (normal) 25

Thought disorder0 (normal) 15

1 (vivid dreaming) 5

2 (benign hallucinations with insight retained) 5

Depression

0 (normal) 24

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

Motivation/Initiative

0 (normal) 20

1 (less assertive than usual; more passive) 3

2 (loss of initiative or disinterest in elective activities) 2

Speech

0 (normal) 14

1 (mildly affected; no difficulty being understood) 8

2 (moderately affected; sometimes asked

to repeat statements)

3

Salivation

0 (normal) 9

1 (slight but definite excess of saliva in mouth;

may have nighttime drooling)

12

2 (moderately excessive saliva;

may have minimal drooling)

4

Swallowing

0 (normal) 20

1 (rare choking) 22 (occasional choking) 2

3 (Requires soft food) 1

138 R. D. Gross et al.: Breathing/Swallowing in Parkinson’s Disease

1 3



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 Parkinson’s

group were analyzed. A total of 214 of 225 cookie swallowswere suitable for analysis from the healthy control group

and 211 of 225 from the Parkinson’s group. Each swallow

was noted by the nearly simultaneous appearance of deg-

lutitive 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 deter-

mined using the combined nasal airflow andplethysmographic signals. When mouth breathing resulted

in a temporary loss of nasal airflow, the signal from pleth-

ysmography 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

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 groupswallowed significantly more often during inhalation,

regardless of whether a semisolid (pudding) or solid

(cookie) was consumed. The IPD participants also exhib-

ited significantly more postswallow inhalation for both

consistencies. In addition, those in the IPD group swal-

lowed both consistencies at low tidal volume significantly

more frequently than those in the control group. Tables 2–4

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 EMGsignal

R. D. Gross et al.: Breathing/Swallowing in Parkinson’s Disease 139

1 3



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 therespiratory cycle, comparisons of DDA for swallows

occurring during inhalation vs. exhalation were also made.

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.

Discussion

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 fluo-

roscopy and showed that inhalation after the swallow

resulted in aspiration, with ‘‘chaotic respiration’’ being

highly associated with aspiration. Recognizing that respi-

ratory 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 oper-

ating 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 swal-

lowing motor control [45–48]. It has been suggested that a

Table 2 Swallow during inhalation

Group Consistency Event/total Odds ratio 95% CI p Value

Healthy Cookie 4/214

IPD Cookie 29/211 8.37 8.9, 24.2 0.0001

Healthy Pudding 22/230

IPD Pudding 39/235 1.9 1.08, 3.20 0.0264

Table 4 Swallow at low tidal volume



IPD Cookie 54/211 2.4 1.43, 3.96 0.0008


IPD Pudding 54/235 4.0 2.21, 7.21 \0.0001

Table 3 Postswallow inhalation



IPD Cookie 52/210 3.2 1.83, 5.57 \0.0001


IPD Pudding 60/235 4.30 2.42, 7.63 \0.0001

Timing of spontaneous swallows within breathing cycle

Heathy controls vs. Parkinson's disease

0

5

10

15

20

25

30

Cookie Pudding Cookie Pudding Cookie Pudding

Swallow during inhalation Inhalation after swallow Low tidal volume

w o l l a

w s f o e g a t n e c r e P

Healthy control

Parkinson's disease

Fig. 2 Percentage of swallows

occurring at times other than the

preferred pattern of exhale-

swallow-exhale: healthy

controls vs. Parkinson’s disease


1 3



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

greater subglottic air pressure during the swallow (deglu-

titive 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 neur-

oregulatory 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 pressurizedlarynx may signal feedback mechanisms related to swal-

lowing 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

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 tra-cheostomy tubes where subglottic air pressure is absent,

but not when the tube is occluded [47, 48, 50–52]. How-

ever, 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 swal-

lowing 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 IPDpatients 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]. Respi-

ratory insufficiency is most likely due to the threefold

nature of the disease’s 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 Parkinson’s disease

also demonstrate voice disorders that are characterized by

reduced loudness and breathiness. These subjective obser-

vations are often indicative of vocal fold bowing and

glottal incompetence [59–61]. The Lee Silverman Voice

Table 5 Duration of deglutitive apnea in milliseconds during exha-

lation vs. inhalation

Group Statistic Exhale DDA Inhale DDA p Value

Healthy N 347 26 0.025

Mean, SD 649, 133 887, 274

Median 670 801

Q1, Q3 609, 748 744, 921Min, Max 377, 1357 576, 1744

Table 6 Duration of deglutitive apnea in milliseconds during exha-

lation vs. inhalation

Group Statistic Exhale DDA Inhale DDA p Value

IPD N 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

Apnea duration of swallows occuring during exhalation vs. inhalation

Exhalation

Exhalation

Inhalation

Inhalation

0

100

200

300

400

500

600

700

800

900

Healthy Parkinson's

s d

n o c e s i l l i M n i n o i t a r u d n a i d e M

Fig. 3 Comparison between the

duration of swallowing apnea

for swallows occurring during

exhalation vs. inhalation


1 3



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 completedby 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 brain’s insular cortex

could have been responsible for the swallowing improve-

ments. Additional plausible explanations are that greater

subglottal pressures were generated not just during pho-

nation [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 Parkinson’s disease group (Fig. 2).

Studies that have compared swallowing physiology under

different respiratory conditions reported significant differ-

ences 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 pro-

vided 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 mid-

exhalation. 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.

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 signifi-

cantly 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 can-

not 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 typ-

ical 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 consis-

tently improve swallowing function or prevent the

development of oropharyngeal dysphagia.


1 3



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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? Yes No

Have you had any difficulty swallowing in the last 6 months other than

a sore throat? Yes No

Have you ever been diagnosed with a stroke or a ministroke? Yes No

Have you ever thought that you had stroke or a ministroke? Yes No

Have you ever had a serious head injury that required a hospital stay? Yes No

Have you ever been diagnosed with a progressive neurological disease

such as Parkinson’s disease, multiple sclerosis (MS), ALS (Lou Gherig’s

disease) or myasthenia gravis? Yes No

Do you think that you have a progressive neurological disease such as

Parkinson’s disease, multiple sclerosis (MS), ALS (Lou Gherig’s disease)

or myasthenia gravis? Yes No

Have you ever been diagnosed with a muscle disease such as polymyositis,

sarcoidosis, myotonic dystrophy, or oculopharyngeal dystrophy? Yes No

Do you think that you might have a muscle disease? Yes No

Have you ever been diagnosed with oral or pharyngeal (throat) cancer? Yes No

Have you ever had an oral or throat tumor removed? Yes No

Have you ever had any surgery to your tongue or to the inside or outside

of your neck? Yes No

Have you ever been diagnosed with chronic obstructive pulmonary disease

(COPD) or emphysema? Yes No

Do you think that you might have chronic obstructive pulmonary disease

(COPD) or emphysema? Yes No

Do you have any difficulty breathing? Yes No


1 3



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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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The Coordination of Breathing and Swallowing in Parkinson’s

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