Swallowing disorders in Parkinsons disease

Abstract

The aim of this study was to assess the reflex and oral, pharyngeal, esophageal phase
of swallowing in patients with Parkinsons disease (PD). Eighteen patients with PD and
22 healthy control subjects were investigated using electromyography (EMG) and
esophageal scintigraphy. This study demonstrated delayed triggering of the swallowing
reflex (443 ^ 84 ms in patients with PD vs. 230 ^ 96 ms in controls, p , 0:05 and
prolongation of laryngeal movement (980 ^ 140 vs. 649 ^ 145 ms, p , 0:05: We found
prolongation of the esophageal phase of swallowing (14.46 ^ 5.30 vs. 7.45 ^ 1.64 s, p ,
0:001 in PD patients. The dysphagia limit i.e. the maximum amount of water
swallowed at once was smaller in PD patients than in controls (6.23 ^ 3.67 vs. .20 ml).
Dysphagia was observed in all patients studied although only 13 of them complained
about it. In the remaining five cases swallowing impairment was subclinical and it
consisted of decreased dysphagia limit and prolongation of the esophageal phase.
Dysphagia at the subclinical level may be one of the early symptoms of PD.

Keywords: Dysphagia; Swallowing disorders; Parkinsons disease; Electromyography;

Scintigraphy

1. Introduction

Swallowing dysfunction often occurs in patients with PD and interferes with their quality
of life [1]. The reported incidence of swallowing dysfunction in PD ranges from 30 to
52%. The symptoms correlate with disease severity and duration [4]. The term
dysphagia characterizes difficulty in swallowing ingested substances and may lead to
malnutrition and aspiration pneumonia or even death [2]. Aspiration may also appear
before patients are able to recognize difficulty swallowing. Therefore, it is important to
evaluate swallowing function before problems arise.

T he act of swallowing may be divided into oral, pharyngeal and esophageal phases
[1,11]. The initial oral phase is mainly voluntary and depends on food consistency,
taste, hunger, and motivation. The pharyngeal phase consists of several coordinated
actions, which transport the food from the oropharynx to the esophagus. These two
phases are interrelated and partially voluntary.

The swallowing reflex is under control of the swallowing center in the brainstem. The
esophageal phase is unconscious and under autonomic control. The cause and
mechanism of dysphagia in PD remain unclear. The aim of this study was the
assessment of oral, pharyngeal and esophageal phases of swallowing in PD patients
compared to controls. Several methods have already been used in the literature for this
purpose manometry [3,11], electromyography (EMG) [58], video fluoroscopy
[11,16,21] and scintigraphy [12,17]. Although disorders of swallowing in PD were
detected in most studies, controversy remains concerning which phase of swallowing is
mainly affected [1,4,15,18]. Therefore, we decided to combine the assessment of
dysphagia limit, EMG technique and scintigraphy, which would allow the investigation
of all phases of swallowing.
2. Material and methods

Eighteen PD patients (12 females and 6 males) and 22 controls (12 females and 10
males) entered the study. The procedure was approved by the Ethical Committee of our
Table 1 university hospital and each subject gave informed consent.

The demographic data of PD patients are presented in Table 1. The severity of PD was
assessed with the use of Hoehn and Yahr scale (H and Y [10] and in addition swallowing
was assessed with the use of Unified Parkinsons Disease Rating Scale (UPDRS) [9]. In
13 patients dysphagia was estimated with the use of UPDRS at 1.62 ^ 0.51. These
patients suffered from cough related to dysphagia, difficulties with food intake and
nausea. Five patients were unaware of any problem swallowing (UPDRS equal 0). All PD
patients were treated with L-dopa in monotherapy (mean daily dose 750 ^ 175 mg)
and they were examined 2 h after medication intake (in the on phase). The mean age
of controls was 70.9 ^ 7.1 and ranged between 56 and 87. It did not significantly differ
from the age of PD patients. None of the controls had any problem with swallowing and
they had no neurological signs or symptoms.

The examination was divided in two parts and evaluated each of three phases of
swallowing. In the first part, we used the modified method of EMG [68]. The second
part consisted of scintigraphy of esophageal activity. Statistical significance was
estimated with the use of Student ttest.

After a clinical neurological examination each of the subjects was sat in an examination
armchair and instructed to hold his/her head in upright position. The EMG electrodes
were taped (A) under chin over the digastric muscle complex, (B) at the level of the
cricoid cartilage, (C) at the coniotomy area and (D) under cornus major of the hyoid
bone. Swallows were initiated with the liquid bolus positioned on the tongue. Swallow
signals were recorded following delivery of 1, 3, 5, 11, 16, 20 ml of water. 20 ml is the
amount of water, which a healthy person can swallow at one time and is called the
dysphagia limit [68]. In dysphagia this parameter is often decreased and subjects
divide the bolus into two or three swallows. Dry swallowing was also investigated in all
subjects. Subsequently, swallowing was assessed with a 3 ml bolus of water. This
amount was used as none of the patients in the study had any difficulty swallowing it.
All the electrodes measured the activity of the muscles, two of them, (B) and (C),
recorded laryngeal movements. The recording time of the signals was 6 s. At least
three successive EMG signals were recorded for each type of swallowing.

In the second part of the study the esophageal transit was estimated using
scintigraphy [12,17] using a Gamma camera (Basicam Siemens). The examination was
performed in the supine position to eliminate the effect of gravity. The patients were
positioned in a way to visualize the mouth, hypopharynx, the entire esophagus, and the
proximal portion of the gastric fundus in the same field. Anterior imaging was routinely
performed. During the examination liquid was given in the form of 510 ml bolus
labeled with 50100 MBq of 99 m Tc-sulfur colloid.

Patients were instructed to retain the bolus in the mouth and to swallow the entire
bolus in one gulp. A high-speed framing rate was used. One set of 64 64 matrix
dynamic images was acquired for total 90 and 0.25 s images were obtained. Separate
regions of interest (ROI) were defined around the oropharyngeal, proximal esophageal,
mdium esophageal and distal esophageal and time-activity curves were generated.
Thereafter, mean transit time was obtained as a difference between maximum activity
in the region of oropharynx and lower part of esophagus.

3. Results

Results for all measured parameters are presented in Tables 2 and 3 as the mean
values ^ standard deviation. The laryngeal movements detected by EMG are shown in
Fig. 1 for PD patients and control subjects. The laryngeal movements signal shows a
pattern of one deflection and it is connected with the passage of the bolus through the
upper esophageal sphincter. The time of this interval is a measure of pharyngeal
transit time. EMG technique evidenced a delay of triggering EMG activity (443 ^ 84 ms
in PD patient vs. 230 ^ 96 ms in controls, the difference being significant at p , 0:05:
The laryngeal movement time was also prolonged in the PD group (980 ^ 140 ms vs.
649 ^ 145 in controls, the difference being significant p , 0:05: The dysphagia limit
was decreased in all PD patients, being 6.23 ^ 3.67 vs. .20 ml in all control subjects
(the difference significant at p , 0:005: The decreased dysphagia limit was observed
also in patients without clinical symptoms of dysphagia (12 ^ 2.73 ml). The dysphagia
limit in this group was higher than in the group with overt clinical swallowing
disorders(4.41 ^ 2.27 ml). The difference between these two PD groups was
statistically significant p , 0:05: Other parameters examined by EMG (time of
triggering and laryngeal movement) in the group without clinical dysphagia did not
differ significantly from those in controls.

Esophageal transit scintigraphy of a PD patient and a control subject is shown in Fig. 2.

The esophageal passage shows a pattern of five deflections. The first one (A) illustrates
the passage of the bolus from the mouth through the upper esophageal sphincter. The
second deflection (B) is a measure of transit through the proximal part of the
esophagus and the third one (C) shows transit in the medium part of the esophagus.
The fourth curve (D) shows passage through the lower esophageal sphincter and the
last one (E) illustrates the presence of the bolus in the stomach.

Prolongation of transit time was observed in PD patients 14.46 ^ 5.3 vs. 7.45 ^ 1.64 s
in controls, with a tendency towards retention in the lower part of the esophagus (8.81
^ 7.12 vs. 6.14 ^ 1.75 s). These differences between the two groups were significant,
p , 0:05: PD patients without clinical dysphagia had a shorter time of esophageal
passage than those with clinical dysphagia (9 ^ 1.4 vs. 17.02 ^ 4.89 s, the difference
being significant at p 14 0:008: The transport time in the lower part of the esophagus
was 8.4 ^ 1.5 s for the first group vs. 13.09 ^ 5.2 s for patients with clinical dysphagia
(the difference significant at, p 14 0:03: This time of passage in the esophagus in both
PD groups was significantly different from that in controls p , 0:05: Patients in the PD
group with clinical dysphagia presented a significantly higher degree of disability
(mean Hand Y score 2.3 ^ 0.5 vs. 1.3 ^ 0.4 for patients with subclinical dysphagia, the
difference significant at p , 0:05: In this group, the duration of disease was longer (6 ^
4.7 years) than in the PD group without clinical dysphagia (5 ^ 2.5 years) although this
difference was not statistically significant p 14 0:27:

4. Discussion
The EMG technique used for the assessment of the swallowing reflex and laryngeal
movements was that used by Ertekin et al. [58]. In those studies prolongation of the
triggering of the swallowing reflex and the duration of laryngeal movement in PD
patients was observed [8]. In our study, we also investigated the esophageal phase of
swallowing. The scintigraphy technique allows the assess ment all of three phases of
swallowing and it adds to the examination of oral and pharyngeal phase by EMG.

Using both these complementary techniques subclinical dysphagia can be uncovered.

Our results demonstrate swallowing disorders in the whole PD group, although five of
the PD patients did not complain of difficulty swallowing. All the patients without
swallowing problems had decreased a dysphagia limit and a prolongation of lower
esophageal bolus transport. The laryngeal movement time was only slightly increased
and this difference was not statistically significant. No prolongation of swallowing reflex
was observed and the oral and pharyngeal transit time was normal. The other 13
patients complained of swallowing disorders i.e. difficulty swallowing solids, pharyngeal
retention, aspiration, heartburn and nausea. All of the PD patients demonstrated an
esophageal phase disorder, although a difference between these two PD groups was
observed.

The mechanism of swallowing disorders in PD may be related to extrapyramidal and

autonomic system disorders. The cardinal symptoms of PDtremor, bradykinesia, and
rigidity are initially responsible for oral dysphagia, which is mainly observed in the
advanced stages of the disease. Pharyngeal dysphagia results from delayed oral
delivery, uncoordination of striated muscles, reduced somatosensory stimuli, (these
factors are strongly connected with the pathology of the oral phase) and abnormal
autonomic function. Degeneration of the dorsal nucleus of the vagus and esophageal
myenteric plexus is responsible for both pharyngeal and esophageal dysphagia [22].
Both swallowing phases are under autonomic control, so the abnormalities of these two
phases may coexist. In our study, we observed esophageal (longer esophageal transit
time) and pharyngeal dysfunction (lower dysphagia limit) in all cases, as well as in
patients with no clinical symptoms of dysphagia. In patients in the advanced stages of
PD, the pharyngeal phase was more disrupted and in addition there was oral
dysphagia.

Our observations show that neurodegeneration in the autonomic nervous system may
occur in the early stages of PD. The comparison between patients with and without
clinical dysphagia suggests that dysphagia is closely connected with the progress of
the disease. Esophageal pathology is an early symptom of dysphagia, which may be
relatively asymptotic. Symptoms of dysphagia are related to disorders of the oral and
pharyngeal phases of swallowing.

Delayed swallowing reflex may be related to the impairment of dopamine metabolism

characteristic for PD. The role of dopamine has been demonstrated in elderly people
withstroke and dysphagia [2,13,14]. It has been shown that Ldopa, amantadine,
angiotensine converting enzyme inhibitors (ACE-I) may improve the swallowing reflex in
patients with basal ganglia infarction [2,14,19,20]. This effect of Ldopa suggest that
dysphagia in PD may be connected with low striatal dopamine concentration. In
conclusion, our study shows that dysphagia is a very frequent symptom of PD although
in the early stages it may be asymptotic. EMG and esophageal scintigraphy may help
to detect dysphagia in cases without any clinical symptoms of it. In individual cases,
this finding may influence the treatment and care, which could prevent the most
common consequences of dysphagia such as pneumonia, aspiration and malnutrition.