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Dysphagia (2008) 23:136–145 DOI 10.1007/s00455-007-9113-4

ORIGINAL ARTICLE

ORIGINAL ARTICLE

The Coordination of Breathing and Swallowing in Parkinson’s Disease

Roxann Diez Gross Æ Charles W. Atwood Jr. Æ Sheryl B. Ross Æ Kimberly A. Eichhorn Æ Joan W. Olszewski Æ 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 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

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: 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

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swallowed significantly more often during inhalation and at low tidal volumes. The Parkinson’s 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 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

dysphagia Swallowing Respiratory control Deglutition Deglutition disorders Subglottic air pressure

Parkinson’s disease Oropharyngeal

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 [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 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

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

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investigations that used fluoroscopy to assess swallowing function with liquids and solids did not determine corre- lation 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 dopa- minergic medication and found that swallowing abnormalities usually persist after the administration of the drug, even when the dose is increased [13, 1517]. Like- wise, 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 dys- phagia 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 dys- kinesia [22, 23], while others report that anti-Parkinson’s 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 breath- ing 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 mid- exhalation has also been reported [28, 31, 33]. Deviation from the normal pattern, particularly postswallow inhala- tion, 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 non- invasive technique. They showed that when given a thin liquid from a spoon, the IPD subjects inhaled after

swallowing significantly more than control subjects. To build upon their findings and gain further insight into the problem, we sought to additionally characterize swallow- ing-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 Parkinson’s 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 System’s Institu- tional 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 = 53–84, 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 partici- pants 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/Initia- tive 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 Retelling–Delayed subtests of the Arizona Battery for Communicative Dis- orders 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

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

Table 1 UPDRS ratings and number of subjects who received each rating

UPDRS scores

No.

subjects

Intellectual impairment

0

(normal)

25

Thought disorder

0 (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

(moderately affected; sometimes asked to repeat statements)

2

3

Salivation

0

(normal)

9

(slight but definite excess of saliva in mouth; may have nighttime drooling)

1

12

(moderately excessive saliva; may have minimal drooling)

2

4

Swallowing

0 (normal)

20

1 (rare choking)

2

2 (occasional choking)

2

3 (Requires soft food)

1

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 FEV 1 /FEV \70%. Individuals

whose delayed/immediate recall ratio was below 95% were

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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 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 swal-

lowing 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 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.

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

139

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 swallows were 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 and plethysmographic 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 group swallowed 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 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

and abdomen band signals that represent tidal volume changes. The box at the bottom shows the

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

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 3 Postswallow inhalation

 

Group

Consistency

Event/total

Odds ratio

95% CI

p Value

Healthy

Cookie

20/214

IPD

Cookie

52/210

3.2

1.83, 5.57 \0.0001

Healthy

Pudding

17/230

IPD

Pudding

60/235

4.30

2.42, 7.63 \0.0001

Table 4 Swallow at low tidal volume

Group

Consistency

Event/total

Odds ratio

95% CI

p Value

Healthy

Cookie

17/214

IPD

Cookie

54/211

2.4

1.43, 3.96

0.0008

Healthy

Pudding

16/230

IPD

Pudding

54/235

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.

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 [4548]. It has been suggested that a

Fig. 2 Percentage of swallows occurring at times other than the preferred pattern of exhale- swallow-exhale: healthy controls vs. Parkinson’s disease

Timing of spontaneous swallows within breathing cycle Heathy controls vs. Parkinson's disease

30 Healthy control Parkinson's disease 25 20 15 10 5 0 Cookie Pudding Cookie Pudding
30
Healthy control
Parkinson's disease
25
20
15
10
5
0
Cookie
Pudding
Cookie
Pudding
Cookie
Pudding
Swallow during inhalation
Inhalation after swallow
Low tidal volume
wollawsfoegatnecreP

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

141

Min sdnocesillininotarudaideM

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, 921

Min, 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

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 pressurized larynx 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, 5052]. 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 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]. 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 [5961]. The Lee Silverman Voice

Fig. 3 Comparison between the duration of swallowing apnea for swallows occurring during exhalation vs. inhalation

Apnea duration of swallows occuring during exhalation vs. inhalation

900

800

700

600

500

400

300

200

100

0

Inhalation Exhalation Exhalation Inhalation
Inhalation
Exhalation
Exhalation
Inhalation

Healthy

Parkinson's

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

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 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.

123

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.

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

143

Appendix A

Screening Questionnaire for Interested Individuals

What happens when you drink thin liquids such as water, coffee, tea or juice?

Subject ID

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

Yes

No

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? Have you ever been diagnosed with a progressive neurological disease such as Parkinson’s disease, multiple sclerosis (MS), ALS (Lou Gherig’s

Yes

No

disease) or myasthenia gravis? Do you think that you have a progressive neurological disease such as Parkinson’s disease, multiple sclerosis (MS), ALS (Lou Gherig’s disease)

Yes

No

or myasthenia gravis? Have you ever been diagnosed with a muscle disease such as polymyositis,

Yes

No

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

Yes

No

of your neck? Have you ever been diagnosed with chronic obstructive pulmonary disease

Yes

No

(COPD) or emphysema? Do you think that you might have chronic obstructive pulmonary disease

Yes

No

(COPD) or emphysema?

Yes

No

Do you have any difficulty breathing?

Yes

No

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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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