ORIGINAL ARTICLE

Swallowing in Patients with Parkinson’s Disease: A SurfaceElectromyography 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 Parkinson’s

disease (PD) patients and normal controls (NC) using sur-

face 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

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 sig-

nificantly 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 Parkinson’s disease � Deglutition � Deglutition

disorders � Dysphagia � Surface electromyography

Parkinson’s 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 Alzheimer’s disease [2]. With the increased aging of

the world’s population, it is estimated that by 2020 more

than 40 million people worldwide will have motor disor-

ders 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 multisys-

temic 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

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

Maurıcio 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 Paraıba, Joao Pessoa, Brazil

O. G Lins

Department of Neuropsychiatry, Federal University of

Pernambuco, Recife, PE 50670-901, Brazil

123

Dysphagia (2012) 27:550–555

DOI 10.1007/s00455-012-9406-0

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 [14–16]. 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 Uni-

versity of Pernambuco (Of. No. 334/2008).

Subjects

The experimental group comprised 15 subjects (7 men)

with PD, aged 45–81 (mean = 63) years, Original Hoehn

and Yahr (HY) Scale [17] I–III, and SWAL-QOL (a

questionnaire to evaluate quality of life in swallowing)

64–96 (mean = 77). Fifteen healthy individuals (3 men)

aged 47–82 (mean = 63) years and SWAL-QOL 80–99

(mean = 91) served as the control group.

The study was done at the Parkinson’s Patient Care Ser-

vice 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 SWAL-

QOL) 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 dis-

posable self-adhesive electrodes (Meditrace 200) fixed to

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 electro-

myograph (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 soft-

ware 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. 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

researcher’s command. Two recordings of each condi-

tion 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 deglu-

tition [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.

2. 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.

M. d. G. WS Coriolano et al.: Swallowing in Parkinson’s Disease 551

123

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 swallow-

ing. Only boluses that were swallowed with a single swallow

were compared to make sure we compared swallowing of

similar volumes.

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 nec-

essary to drink the full volume.

Data were summarized as means and standard devia-

tions. 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) swal-

lowing of 10 ml of water and yogurt. For the drinking

condition a Student’s t test was used to compare the time

each group took to drink 100 ml of water and the Mann-

Whitney test was used to compare the number of swallows.

Statistical significance was considered if p B 0.05.

Results

Swallowing Condition

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 mul-

tiple 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

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 signifi-

cantly 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

Table 1 Number and percentage of Parkinson’s 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 Parkinson’s

(%)

Normal

(%)

p Kappa

Water 10 54 7 \0.001* 0.47

20 80 20 \0.001** 0.60

Yogurt 5 73 0 \0.001* 0.73

10 73 20 \0.001** 0.53

*Fischer exact test

**v2 test

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) Single swallow

Parkinson n Normal n

Water 10 2.2 (0.6) 7 1.7 (0.3) 14

20 2.9 (0.8) 3 2.2 (0.6) 7

Yogurt 5 4.0 (1.7) 4 2.1 (0.4) 15

10 3.5 (1.2) 4 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 sig-

nificant; main effect for volume significant; interaction non-signifi-

cant. (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

552 M. d. G. WS Coriolano et al.: Swallowing in Parkinson’s Disease

123

and PD subjects. Durations were significantly longer dur-

ing 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 lar-

ger during swallowing of 20 ml of water than for swal-

lowing 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 vol-

ume of water per swallow (in milliliters), calculated by

dividing 100 ml by the number of swallows each subject

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

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 con-

sistencies and volumes. This finding is consistent with the

results obtained by other authors. In studying the swal-

lowing 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 dis-

cussion 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

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) Parkinson’s n Normal n

Water 10 17 (7) 7 19 (8) 14

20 23 (9) 3 22 (7) 7

Yogurt 5 23 (8) 4 23 (7) 15

10 l 22 (9) 4 25 (8) 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 non-

significant; main effect for volume significant; interaction non-sig-

nificant. (2) Swallowing of yogurt: main effect for condition non-

significant; main effect for volume non-significant; interaction non-

significant. (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 (4–7)

Parkinson’s disease 23 (13) 7 (4–11)

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

(range)

t test: time to swallow 100 ml significantly different

M. d. G. WS Coriolano et al.: Swallowing in Parkinson’s Disease 553

123

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 dis-

crepancies 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 dif-

ferences 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

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 character-

istics of the bolus [27–29]. 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 drink-

ing). 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.

554 M. d. G. WS Coriolano et al.: Swallowing in Parkinson’s Disease

123

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 poten-

tially useful finding. For example, is there a relationship

between the average volume per swallow and the dyspha-

gia 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 The authors have no conflicts of interest to

disclose.

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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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