Dysphagia (2012) 27:550555

DOI 10.1007/s00455-012-9406-0

ORIGINAL ARTICLE

Swallowing in Patients with Parkinsons Disease: A Surface

Electromyography Study
Maria das Gracas WS Coriolano Luciana R Belo
Danielle Carneiro Amdore G Asano Paulo Jose AL Oliveira
Douglas Monteiro da Silva Otavio G Lins

Received: 26 September 2011 / Accepted: 12 March 2012 / Published online: 27 May 2012
Springer Science+Business Media, LLC 2012

Abstract Our goal was to study deglutition of Parkinsons

disease (PD) patients and normal controls (NC) using surface electromyography (sEMG). The study included 15
patients with idiopathic PD and 15 age-matched normal
controls. Surface electromyography was collected over the
suprahyoid muscle group. Conditions were the following:
swallow at once 10 and 20 ml of water and 5 and 10 ml of
yogurt of firm consistency, and freely drink 100 ml of water.
During swallowing, durations of sEMG were significantly
longer in PD patients than in normal controls but no
M. d. G. WS Coriolano
Department of Anatomy, Federal University of Pernambuco,
Cidade Universitaria, Recife, PE 50670-901, Brazil
L. R Belo
D. M. da Silva
Neuropsychiatry and Behavioural Sciences Postgraduation
Program, Federal University of Pernambuco, Brazil, Recife,
PE 50670-901, Brazil
A. G Asano
Pro-Parkinson service, Clinical Hospital, Federal University
of Pernambuco, Recife, PE 50670-901, Brazil
P. J. AL Oliveira
Maurcio de Nassau College, Recife, Brazil, Rua Guilherme
Pinto, 114 Gracas, Recife, PE, Brazil
M. d. G. WS Coriolano (&)
Rua Professor Antonio Coelho, 694, Apt. 102,
Varzea 50740-020, Brazil
e-mail: gracawander@hotmail.com
D. Carneiro
Department of Occupational Therapy, Federal University
of Paraba, Joao Pessoa, Brazil
O. G Lins
Department of Neuropsychiatry, Federal University of
Pernambuco, Recife, PE 50670-901, Brazil

123

significant differences of amplitudes were found. Eighty

percent of the PD patients and 20 % of the NC needed more
than one swallow to consume 20 ml of water, while 70 % of
the PD patients and none of the NC needed more than one
swallow to consume 5 ml of yogurt. PD patients took significantly more time and needed significantly more swallows
to drink 100 ml of water than normal controls. We conclude
that sEMG might be a simple and useful tool to study and
monitor deglutition in PD patients.
Keywords Parkinsons disease
Deglutition
Deglutition
disorders
Dysphagia
Surface electromyography

Parkinsons disease (PD) is a progressive neurological

disease that affects 0.3 % of the general population [1] and
is the second most common neurodegenerative disease
after Alzheimers disease [2]. With the increased aging of
the worlds population, it is estimated that by 2020 more
than 40 million people worldwide will have motor disorders as a consequence of PD [3]. However, its etiology is
still unknown in most occurrences [4].
There is a combination of signs and symptoms, both
motor and nonmotor, which characterize PD as a multisystemic disease. The cardinal motor symptoms are tremors,
rigidity, bradykinesia, and postural dysfunctions [5]. Among
the nonmotor symptoms, neuropsychiatric dysfunctions,
sleep disorders, autonomic dysfunctions, and some sensory
dysfunctions have been described [4, 6]. These features are
well known and particularly evident in the late stages of the
disease; however, there is growing evidence that a number of
symptoms can precede the classical motor features of PD,
defining a period known as the premotor phase of the disease
[7]. PD shows heterogeneity in clinical presentation,
response to therapy, and the rate of disease progression,

M. d. G. WS Coriolano et al.: Swallowing in Parkinsons Disease

which can be fast or slow [8]. While the beginning of

symptoms usually occurs at the age of 65, it can start before
that age [7].
A crucial aspect related to the quality of life of patients
with PD is deglutition disorder (dysphagia). Dysphagia is a
common dysfunction in PD and is considered an important
cause of low quality of life and death by aspiration [9, 10].
Videofluoroscopy is considered the gold-standard method to
evaluate deglutition [11, 12]. However, this is an expensive
method and cannot be performed frequently [13]. Due to
this, some authors suggest surface electromyography
(sEMG) as a noninvasive, inexpensive, and easily repeatable
test to study deglutition in PD [1416]. The aim of this work
was to study the deglutition of patients with PD and normal
controls using surface electromyography (sEMG). Our
hypothesis is that sEMG may be useful for evaluating
deglutition in patients with Parkinson disease.

Methods
This study was approved by the Human Research Ethics
Committee of Health Science Center of the Federal University of Pernambuco (Of. No. 334/2008).
Subjects
The experimental group comprised 15 subjects (7 men)
with PD, aged 4581 (mean = 63) years, Original Hoehn
and Yahr (HY) Scale [17] IIII, and SWAL-QOL (a
questionnaire to evaluate quality of life in swallowing)
6496 (mean = 77). Fifteen healthy individuals (3 men)
aged 4782 (mean = 63) years and SWAL-QOL 8099
(mean = 91) served as the control group.
The study was done at the Parkinsons Patient Care Service and at the Clinical Neurophysiology Laboratory of the
Clinical Hospital of the Federal University of Pernambuco,
Brazil, from October 2008 to May 2009. The patients were
invited to participate in the study during consultation. The
inclusion criteria of individuals with PD were the following:
(1) diagnosis of idiopathic PD; (2) normal dental elements or
well-adapted dental prosthesis; and (3) being in stage I, II, or
III of the disease, according to the HY Scale [17]. Individuals
with cognitive deficits (screened with the mini-mental test)
and/or risk of bronchoaspiration (screened with the SWALQOL) were excluded from the study. The individuals of the
control group were generally the companions of the PD
patients. All participants signed an informed consent form.
Recordings
The electrical activity of muscles was recorded using disposable self-adhesive electrodes (Meditrace 200) fixed to

551

the skin. Before attaching the electrodes, the skin was

cleaned with gauze embedded with 70 % alcohol and
slightly abraded with abrasive paste (NuPrep). A pair of
self-adherent electrodes was attached symmetrically under
the suprahyoid muscle group, below the chin, 1 cm to the
left, and 1 cm to the right from the midline. The ground
electrode was attached to the skin over the right clavicle.
The signal registered by the electrodes was amplified
(2,000 times), filtered (high-pass 20 Hz, low-pass 2 kHz), and
digitized (8 kHz, 2 kHz per channel) by a surface electromyograph (EMG Systems do Brazil, model EMG 400c).
The recordings were saved as text files. A dedicated
program developed in our laboratory [16] and written in
MATLABTM (MathWorks, Natick, MA, USA) was used to
analyze the surface electromyograms (sEMG). This software reads the raw data, removes the offset, rectifies the
signal, and calculates the root-mean-square (rms) amplitude
in a nonsuperimposed moving window of 100 ms (200
points). The resulting curves are shown on the screen so the
investigator can select with the mouse the beginning and the
end of the sEMG during swallowing. The software calculates
the duration and the average rms amplitude of the sEMG.
Recording Protocol
Recordings were done under two conditions:
1.

2.

Swallowing condition: Swallowing of 10 and 20 ml of

water and 5 and 10 ml of yogurt. The volume was placed
in the mouth with a plastic syringe and the subject kept
the volume in the mouth, swallowing only at the
researchers command. Two recordings of each condition were obtained for all swallowing conditions. Most
times we analyzed the first recording. In 5 % of the
times the recordings were not technically good so we
used the second recording. The volume of 20 ml of
water was chosen because this volume is considered the
dysphagia limit or the lower limit of piecemeal deglutition [13, 14, 18, 19]. The volume of 10 ml was chosen
because it is half of this volume. In a pilot study we
noticed that the subjects had difficulty in keeping 20 ml
of yogurt in the mouth; therefore, we decided to use the
volumes of 10 and 5 ml for yogurt. The command to
swallow was given 2 s after the beginning of the
recording.
Drinking condition: Sequential swallowing of 100 ml
of water. A disposable plastic glass containing 100 ml
of water was given to the subject and she/he was
instructed to drink it normally, when ordered. Free
drinking of 100 ml of water was used by Vaiman [20
23] in his studies of standardization of sEMG. Total
analysis time was 30 s. The command to drink was
given 2 s after starting the recording.

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552

Measurement Procedure
The onset of swallowing was considered to be when the
sEMG activity rose clearly above the background activity
preceding. The end of swallowing was scored when the
EMG activity returned to levels of background activity. The
difference between the beginning and end of swallowing
determines the duration of sEMG activity during swallowing. Only boluses that were swallowed with a single swallow
were compared to make sure we compared swallowing of
similar volumes.

M. d. G. WS Coriolano et al.: Swallowing in Parkinsons Disease

Table 1 Number and percentage of Parkinsons patients and normal
subjects who presented more than one peak during swallowing 10 and
20 ml of water and 5 and 10 ml of yogurt
Condition Volume Parkinsons
(%)
Water
Yogurt

Normal
(%)

10

54

20

80

20

73

10

73

20

Kappa

\0.001*

0.47

\0.001** 0.60
\0.001*

0.73

\0.001** 0.53

*Fischer exact test

**v2 test

Data Analysis
Data were tabulated in Microsoft ExcelTM spreadsheets
(Microsoft Corp., Redmond, WA, USA) and analyzed
using Medicalc statistical software (MedCalc Software,
Mariakerke, Belgium). For the swallowing condition, the
variables studied were amplitude (lV) and duration (in
seconds). For the free-drinking condition, the variables
studied were time to drink and number of swallows necessary to drink the full volume.
Data were summarized as means and standard deviations. For the swallowing conditions, two-way (2 groups by
2 volumes or consistencies) mixed-model ANOVA models
were used for comparing the amplitudes and durations of
sEMGs during (1) swallowing of 10 and 20 ml of water,
(2) swallowing of 5 and 10 ml of yogurt, and (3) swallowing of 10 ml of water and yogurt. For the drinking
condition a Students t test was used to compare the time
each group took to drink 100 ml of water and the MannWhitney test was used to compare the number of swallows.
Statistical significance was considered if p B 0.05.

peaks. During the swallowing of 20 ml of water, 80 % of

the PD patients and 20 % of the normal subjects showed
more than one peak (60 % two peaks and 20 % three peaks
for the PD patients and 13 % two peaks and 7 % three
peaks for the normal subjects). For the swallowing of
yogurt, 73 % of the PD patients presented more than one
peak (60 % two peaks and 13 % four peaks) for both 5 and
10 ml, while 0 and 20 % of the normal subjects presented
more than one peak (13 % two peaks and 7 % three peaks)
during the swallowing of 5 and 10 ml, respectively.
Duration
Table 2 gives the durations of the sEMG during the
swallowing condition. Durations were significantly longer
for PD subjects than for normal subjects, for all tested
volumes and consistencies. Durations were also significantly longer for the swallowing of 20 ml of water than for
swallowing 10 ml, but were not significantly different for
the swallowing of 5 and 10 ml of yogurt, for both normal

Results
Swallowing Condition

Table 2 Durations (in seconds) of the sEMG during swallowing of

10 and 20 ml of water and 5 and 10 ml of yogurt
Condition

Volume (ml)

Number of peaks during swallowing

Table 1 shows the number and percentage of PD patients
and normal subjects who presented more than one peak
during swallowing 10 and 20 ml of water and 5 and 10 ml
of yogurt. Most of the PD patients presented multiple
sEMG peaks during swallowing of all tested volumes and
consistencies, while only a few of the normal subjects
presented more than one peak. Association between multiple peaks and PD was statistically significant. Kappa
coefficient of association was larger for the swallowing of
5 ml of yogurt (0.73), followed by 20 ml of water (0.63).
During the swallowing of 10 ml of water, 54 % of the
PD patients and 7 % of the normal subjects presented two

123

Single swallow
Parkinson

Water
Yogurt

Normal

n
14

10

2.2 (0.6)

1.7 (0.3)

20

2.9 (0.8)

2.2 (0.6)

4.0 (1.7)

2.1 (0.4)

15

10

3.5 (1.2)

2.5 (0.7)

12

Values are given are mean (SD)

Only boluses that were swallowed with a single swallow were
analyzed
ANOVAs: (1) Swallowing of water: Main effect for condition significant; main effect for volume significant; interaction non-significant. (2) Swallowing of yogurt: main effect for condition significant;
main effect for volume non-significant; interaction non-significant.
(3) Comparison of consistencies: main effect for condition significant;
main effect for consistency significant; interaction non-significant

M. d. G. WS Coriolano et al.: Swallowing in Parkinsons Disease

553

and PD subjects. Durations were significantly longer during swallowing of 10 ml of yogurt than an equal volume of
water, in both normal and PD subjects.
Amplitudes
Table 3 shows the amplitudes of the sEMG during the
swallowing conditions. Amplitudes were not significantly
different between normal and PD subjects for any tested
volume or consistency. Amplitudes were significantly larger during swallowing of 20 ml of water than for swallowing 10 ml, but were not significantly different during
swallowing of 10 and 5 ml of yogurt, in both normal and
PD subjects. Amplitudes were significantly larger during
the swallowing of 10 ml of yogurt than an equal volume of
water, in both normal and PD subjects.
Drinking (Sequential Swallowing) Condition
Table 4 shows the time (in seconds) and the number of
swallows the normal and PD subjects took to drink 100 ml
of water. The table also shows the estimated average volume of water per swallow (in milliliters), calculated by
dividing 100 ml by the number of swallows each subject
Table 3 Amplitudesrms (lV) of the sEMG during swallowing of 10
and 20 ml of water and 5 and 10 ml of yogurt
Single swallow
Condition

Volume (ml)

Parkinsons

Normal

17 (7)

19 (8)

14

needed to drink the full volume. PD subjects needed a

larger number of swallows (median = 7 vs. 5; Mann
Whitney U test, p = 0.017) and took significantly more
time (mean = 23 vs. 12 s; t test, p = 0.004) to drink
100 ml of water than normal subjects.

Discussion
Multiple Peaks and Piecemeal Deglutition
Most PD subjects and some normal subjects presented two or
more peaks of the sEMG during swallowing. This was most
obvious during the swallowing of 20 ml of water. Ertekin
et al. [13] recorded suprahyoid sEMG during swallowing of
increasing volumes of water. For volumes above 20 ml,
normal subjects tended to divide the bolus into two or more
parts; this is called piecemeal or in-parts deglutition.
This volume (20 ml) is known as the dysphagia limit,
which is reduced in PD patients [13, 14, 19].
The multiple peaks we observed probably represent
piecemeal deglutition. In the normal subjects multiple
peaks occurred mainly during the swallowing of 20 ml of
water and 10 ml of yogurt (both in 20 % of the subjects),
whereas in the DP patients it occurred in 50 and 80 % of
the subjects during the swallowing of 10 and 20 ml of
water, respectively, and in 70 % during the swallowing of
either 5 or 10 ml of yogurt.
Duration

Water
Yogurt

10
20

23 (9)

22 (7)

5
10 l

23 (8)
22 (9)

4
4

23 (7)
25 (8)

15
12

Values are given are mean (SD)

Only boluses that were swallowed with a single swallow were
analyzed
ANOVAs: (1) Swallowing of water: main effect for condition nonsignificant; main effect for volume significant; interaction non-significant. (2) Swallowing of yogurt: main effect for condition nonsignificant; main effect for volume non-significant; interaction nonsignificant. (3) Comparison of consistencies: main effect for condition
non-significant; main effect for consistency significant; interaction
non-significant

Table 4 Sequential swallowing of 100 ml of water

Conditions

Time to drink
100 ml (s)

No. of swallows

Normal controls

12 (5)

5 (47)

Parkinsons disease

23 (13)

7 (411)

Time values are mean (SD); the number of swallows is median

(range)
t test: time to swallow 100 ml significantly different

The duration of sEMG is the time needed to complete a

cycle of activation of a muscle or a muscle group. The
duration of the suprahyoid sEMG is an important piece of
information and is often used to establish the beginning and
the end of the oropharyngeal phase of a swallow [13, 18].
In our cohort the duration of sEMG was significantly
longer in PD patients than in normal controls for all consistencies and volumes. This finding is consistent with the
results obtained by other authors. In studying the swallowing of water in normal and PD subjects, Ertekin [13,
18], Potulska [19], and Alfonsi [15] found that the duration
of electromyographic activity is significantly longer in PD
patients. The durations obtained by them were generally
somewhat shorter than ours, probably because they used
smaller bolus volumes: Ertekin and Potulska used 3 ml and
Alfonsi 2 ml, while we used 10 and 20 ml (see the discussion below on the effect of volume). A disorder that
increases the duration of the activity of a muscle and/or
disturbs the sequential activation of the several muscles
involved in swallowing may increase the duration of the
sEMG [24]. The larger duration of sEMG in the PD group
is probably related to bradykinesia and/or incoordination of

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554

the muscles involved in the swallowing process in the PD

patients.
The duration of the sEMG was significantly longer for
swallowing 20 ml than for swallowing 10 ml of water for
both normal and PD subjects. No significant differences
were found between durations of the sEMG for 5- and
10-ml swallowings of yogurt in normal or PD subjects.
Ertekin et al. [25, 26] found a significant increase in the
duration of the suprahyoid sEMG with the increase in the
volume (3, 10, and 20 ml) of water or semisolids, while
Dantas et al. [27] found no significant differences in the
duration of suprahyoid sEMG during of 2-, 5-, 10-, and
20-ml swallowings of liquid and pasty barium. These discrepancies may be related to subject and/or methodological
differences. For example, Dantas studied 9 subjects, while
Ertekin studied 14 and we studied 15 subjects. Dantas used
liquid barium while Ertekin and we used water.
The duration of the sEMG was significantly longer for
swallowing 10 ml of yogurt than for swallowing an equal
volume of water for both normal and PD subjects. This is
consistent with the findings of Dantas [27] (longer sEMGs
for the swallowing of equal volumes of pasty rather than
liquid barium), Ruark et al. [28] (longer durations of sEMGs
for swallowing equal volumes of consistent food than of
water), and Taniguchi et al. [29] (direct relationship between
food consistency and duration of the sEMG). Quantitative
comparisons among the data are complicated by the multiple
types of consistencies used in the studies [29].
Amplitudes
Amplitudes of single-bolus analysis in sEMG should be
carefully evaluated because the amplitude of the submental
muscle group might be variable from swallow to swallow in
normal subjects and various groups of neurogenic dysphagia.
In our study there were no statistically significant differences in amplitudes between normal and PD subjects for
any tested volumes or consistencies. Ertekin et al. [18],
studying the swallowing of 3 ml of water in normal and PD
subjects, also did not find significant differences between
the amplitudes of the suprahyoid sEMG for PD patients
and normal controls.
The amplitudes of sEMG were significantly larger for
the swallowing of 20 of water than for swallowing 10 ml in
both normal and PD subjects. Dantas et al. [27] found no
significant differences in the amplitude of suprahyoid
sEMG during the swallowing of 2, 5, 10, and 20 ml of
liquid and pasty barium. The reason for this discrepancy is
not known and may be related to the specific subject or
methodological differences. For example, Dantas et al. [27]
studied young healthy subjects while we studied older
normal and PD subjects. The volume and consistency of
the bolus are sensed by many mechanical and chemical

123

M. d. G. WS Coriolano et al.: Swallowing in Parkinsons Disease

receptors located on the tongue and pharynx, and this

information acts as a feedback mechanism that affects the
central motor programming of swallowing, adjusting the
action of swallowing with the physicochemical characteristics of the bolus [2729]. Aging might decrease the
sensitivity of the tongue and pharynx to the bolus and/or
alter the central mechanisms involved in swallowing.
The amplitudes of the sEMG during the swallowing of
equal volumes of water and yogurt (10 ml) were significantly
larger for the swallowing of yogurt in both normal and PD
subjects. This is consistent with the finding of other authors. In
the study by Dantas et al. [27], the amplitude of suprahyoid
sEMGs was significantly larger for the swallowing of pasty
rather than liquid barium. Ruark et al. [28] found that the
amplitudes of suprahyoid sEMGs were significantly larger in
the swallowing of equal volumes (3 cc) of consistent food
(cottage cheese, pudding, thick liquid) rather than water.
Taniguchi et al. [29] found a direct relationship between the
food consistency and the amplitude of sEMG.
Free Swallowing of 100 ml of Water
The PD subjects required a significantly longer time and a
larger number of swallows to drink 100 ml of water than
normal subjects. There are not many studies that have
evaluated sequential swallowings of water, especially in
PD. There are some studies on sequential swallowings by
videofluoroscopic methods since Daniels and Foundas [30].
The 3-oz water-swallowing test, a kind of clinical
sequential swallowing, has been used in many patients with
neurogenic dysphagia [31]. It is important to study sEMG
for sequential water swallowings of 100 ml water together
with respiratory devices to find whether aspiration occurs.
Study of sequential 100-ml water swallowings from a cup
using sEMG has been recently demonstrated in motor
neuron disease and PD [32]. In a study with 440 normal
adults, the time required for the swallowing of the volume
tended to increase with age [20, 21]. The measures of time
in these studies were similar to ours at similar ages.
The number of swallows during water drinking and the
total duration of continuous drinking of 100 ml of water
are useful parameters for studying swallowing [32]. From
these measurements we perhaps could derive more
functional parameters such as an average duration of
the swallowing cycle (by dividing the total duration of
continuous drinking by the number of swallows during
drinking) and an average volume per swallow (by
dividing 100 ml by the number of swallows during drinking). Those are only average parameters. It would probably
also be important to calculate measurements of variability,
regularity, and rhythmicity of the sequential swallows [32].
However, specific studies are necessary to test these
suppositions.

M. d. G. WS Coriolano et al.: Swallowing in Parkinsons Disease

In our data the mean average duration of the swallowing

cycle and average volume per swallow were 2.3 s and
19 ml for normal controls and 3.3 s and 19 ml for the PD
patients, respectively. This was an interesting and potentially useful finding. For example, is there a relationship
between the average volume per swallow and the dysphagia limit? More specific studies on this matter are necessary
and are underway in our laboratory.
Conclusion
Surface EMG might be a simple and useful tool to study
and monitor deglutition in PD patients. The most efficient
parameters for differentiating normal and PD patients are
(1) the duration of single swallows and the occurrence of
multiple swallows during swallowing of small volumes of
water and yogurt, and (2) the number of swallows and the
time necessary to drink 100 ml of water.
Conflict of interest
disclose.

The authors have no conflicts of interest to

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Maria das Gracas WS Coriolano

PhD

Luciana R Belo MSc

Danielle Carneiro

MSc

Amdore G Asano

MSc

Paulo Jose AL Oliveira

Douglas Monteiro da Silva
Otavio G Lins

PhD

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