Dysphagia in Duchenne Muscular Dystrophy Assessed Objectively by Surface Electromyography

ORIGINAL ARTICLE

Dysphagia in Duchenne Muscular Dystrophy Assessed Objectivelyby Surface Electromyography

Sally K. Archer • Rachel Garrod •

Nicholas Hart • Simon Miller

Received: 21 September 2011 / Accepted: 5 October 2012 / Published online: 21 November 2012

� Springer Science+Business Media New York 2012

Abstract Objective swallowing assessment is indicated in

the management of patients with Duchenne muscular dys-

trophy (DMD). Surface electromyography (sEMG) provides

a non-invasive, objective method of quantifying muscle

activity. It was hypothesised that the measurement of sEMG

activity during swallowing would distinguish between pre-

served and disordered swallow function in DMD. This

comparative study investigated the peak, duration, and rel-

ative timing of muscle activity during swallowing of four

muscle groups: orbicularis oris, masseter, submental, and

infrahyoid. The study included three groups of participants:

Nine DMD patients with dysphagia (mean age = 21.7 ±

4.2 years), six DMD patients with preserved swallow func-

tion (21.0 ± 3.0 years), and 12 healthy controls (24.8 ±

3.1 years). Dysphagic DMD participants produced signifi-

cantly higher normalised peak amplitude measurements than

the healthy control group for masseter (61.77 vs. 5.07;

p B 0.01) and orbicularis oris muscles (71.87 vs. 26.22;

p B 0.05). Intrasubject variability for masseter peak

amplitude was significantly greater for dysphagic DMD

participants than the other groups (16.01 vs. 5.86 vs. 2.18;

p B 0.05). There were no differences in timing measure-

ments between groups. Different characteristic sEMG

waveforms were observed for the three groups. sEMG pro-

vides useful physiological information for the evaluation of

swallowing in DMD patients, justifying further study.

Keywords Deglutition � Deglutition disorders �Dysphagia � Duchenne muscular dystrophy �Surface electromyography (sEMG) � Assessment �Neuromuscular disease

Duchenne muscular dystrophy (DMD) is the most common

childhood onset neuromuscular disorder and leads to

degeneration of muscle fibres and progressive muscle

weakness and death, usually when the patient is in his 20s [1].

Dysphagia is common in DMD, contributing to both mor-

bidity and mortality and accelerating respiratory decline [2].

Following a Cochrane review in 2004, which recommended

the establishment of appropriate swallowing assessments for

patients with chronic muscle disease [2], a series of studies

have used videofluoroscopy and questionnaires to investi-

gate dysphagia in DMD [3–6]. All studies have shown that

dysphagia worsens with age, with increasingly effortful

mastication, reduced hyolaryngeal movement, and poor

pharyngeal clearance, all attributed to progressive oropha-

ryngeal weakness. A discrepancy between findings on vid-

eofluoroscopy and subjective accounts has been reported,

with patients often underreporting the difficulties observed

on assessment [3–5]. These findings all suggest the need for

detailed, reproducible, objective swallowing assessments

that can quantify and regularly monitor the patients, who

may themselves be unaware of their own difficulties.

S. K. Archer (&)

Centre for Human and Aerospace Physiological Sciences,

School of Biomedical Sciences, King’s College London,

Guy’s Campus, London SE1 1UL, UK

e-mail: [email protected]

S. K. Archer � N. Hart

National Institute for Health Research (NIHR) Biomedical

Research Centre, Guy’s and St Thomas’ NHS Foundation Trust

and King’s College London, London, UK

R. Garrod

Physiotherapy Department, King’s College Hospital NHS

Foundation Trust, Denmark Hill, London, UK

S. Miller

62 Southfield Road, Nailsea BS48 1JD, UK

123

Dysphagia (2013) 28:188–198

DOI 10.1007/s00455-012-9429-6

Proactive management is recommended for DMD

patients [1] and requires appropriate and timely assessment.

The commonly applied swallowing assessments, e.g., the

bedside swallow assessment, videofluoroscopy and

fibreoptic endoscopic evaluation of swallowing (FEES), are

clinically valuable; however, none provides an easily

accessible, consistently reliable, and objective measure of a

patient’s swallow function. Surface electromyography

(sEMG) is a noninvasive technique that enables measure-

ment of muscle activity [7]. Previous data have shown that it

provides consistent results during swallowing [8], and peaks

in sEMG activity correlate with key swallowing events [9].

The method is easy to administer, can be used while patients

swallow normal food and fluids, and is well tolerated [10]. It

is therefore potentially useful for both single and serial

assessments, enabling the clinician to track change in a

patient’s muscle function over time. Thus, it could be ideally

suited to monitoring swallowing in progressive neuromus-

cular disease, enabling proactive management.

Despite this, there are limited data on the clinical appli-

cation of sEMG in swallowing assessment and, in particular,

on reporting its ability to distinguish between patients with

and without oropharyngeal dysphagia. Although a few

studies have attempted to produce normal ranges for sEMG

during swallowing, [11, 12], their data were not normalised,

which is a major limitation for clinical comparison. As with

other physiological measurements, sEMG activity must be

normalised or scaled against a reference measurement to

provide a meaningful comparison between subjects. This is

to counterbalance the changes in the signal amplitude which

are dependent on the anatomical recording site, extent of skin

preparation, the depth of subcutaneous tissue between the

skin and the muscles, and any variations in the geometry of

action potentials in the muscle with respect to the recording

electrodes [13].

No previous study has investigated the clinical useful-

ness of sEMG in the assessment of swallowing in DMD.

With multichannel sEMG, it is possible to assess several

groups of muscles simultaneously and, therefore, examine

both oral and pharyngeal muscle groups for signs of

myopathy. Previous electromyographic studies of limb

muscles in patients with myopathy reported a reduction in

electromechanical efficiency due to atrophy of muscle

fibres, with patients needing to activate more motor units

with a resultant increase in amplitude of activity to produce

a given force [14]. Furthermore, a decrease in the mean

duration of motor unit action potentials has been found,

reflecting the diffusely distributed loss of muscle fibres

within the motor unit [14–16]. It was therefore hypothe-

sised that sEMG assessment of dysphagic DMD patients

would demonstrate signs of myopathy in the muscles that

are active during swallowing. Specifically, dysphagic

DMD patients would produce increased muscle activity for

swallowing (relative to their maximum activity) compared

to healthy controls, and the activity would be shorter in

duration. It was anticipated that patients with DMD and

preserved swallow function are yet to develop these myo-

pathic changes to their swallowing muscles and therefore

their sEMG data would be comparable with that of healthy

controls. As such, it was hypothesised that non-invasive

measurement and quantification of swallow function by

sEMG would be able to distinguish between DMD patients

with preserved and disordered swallow function.

Methods

Study Design

A prospective, controlled, cross-sectional study was con-

ducted. Ethical approval was obtained from the Royal

Marsden Research Ethics Committee, and Research and

Development (R&D) approval was obtained from the

Guy’s and St Thomas’ R&D department. All participants

gave written informed consent.

Participants

Healthy Volunteers

Male students attending St George’s, University of Lon-

don, were recruited by advertisement. Inclusion criteria

were males aged 16–30 years. Exclusion criteria included

a history of neurological or neuromuscular disease and

dysphagia.

Patient Volunteers

Participants with DMD were recruited from the Lane Fox

Respiratory Unit Outpatient Clinic at St Thomas’ Hospital,

London. Inclusion criteria were a diagnosis of DMD and

age over 16 years. Exclusion criteria included a diagnosis

of any other neurological or neuromuscular disease and

cognitive impairment preventing informed consent. DMD

participants with a clinical history of dysphagia, as deter-

mined from the medical notes and speech and language

therapy database and a Functional Oral Intake Score

(FOIS) [17] of B6, were assigned to Group 1 and those

with no history of dysphagia, who had preserved swallow

function and FOIS of 7, were assigned to Group 2.

Study Protocol

Each participant’s data were collected in a single session of

less than 20 min. During the session, the DMD participants

remained in their usual seated position in their wheelchairs

S. K. Archer et al.: Dysphagia in Duchenne Muscular Dystrophy Assessed Objectively 189

123

and the control group participants were comfortably seated

upright on a plinth with a supporting back rest. Four

miniature preamplifiers [18] were used to record the sur-

face electromyogram of orbicularis oris muscle, masseter

muscle, infrahyoid muscles, and the submental muscle

group. The characteristics of the preamplifiers [18] were

gain of 91,000, common mode rejection ratio of

80–100 dB in the range 50–500 Hz, and frequency

response of 10–1,000 Hz. Prior to electrode placement, the

skin surface was prepared by shaving and then light abra-

sion with NuPrep skin preparative gel (Pulse Medical,

Surrey, UK). The preamplifiers were attached to the skin

with double-sided adhesive foam tape (3M Ltd, Bracknell,

UK). The recording electrodes were 5-mm-diameter Ag/

AgCl discs set in the plastic preamplifier housing, with

centres separated by 20 mm. A third electrode in the

housing acted as a virtual earth. Holes were punctured in

the foam tape, with the holes corresponding with the

electrodes, and were filled with Ten20 conductive paste

(Pulse Medical) to ensure skin contact. The preamplifiers

were then further secured in place on the skin with

Micropore surgical tape (MidMeds, Waltham Abbey, UK).

The placement of the electrodes had the same anatomical

coordinates as described in previous studies [10, 19], which

was confirmed by palpation of each muscle group while the

participant performed the different maximum voluntary

contractions (see below). Electrode placement was always

on the left side and in the vertical plane, as follows:

1. Orbicularis oris: One recording electrode placed

above the upper lip and one below the lower lip, with

the virtual ground lateral to the vermillion border at the

corner of the mouth.

2. Masseter: Electrodes placed vertically along the

masseter muscle.

3. Submental muscles: Electrodes placed midway

between the mandible and the hyoid bone, 1 cm from

midline.

4. Infrahyoid muscles: Electrodes placed lateral to the

thyroid cartilage.

The analogue signals were digitized at 1 kHz and cap-

tured by a data acquisition device [model 1401, Cambridge

Electronic Design (CED), UK] and recorded for sub-

sequent analysis with Spike 2 software ver. 5.20 (CED).

Sampling rate for all four channels was 1,000 Hz. The

signals were rectified and low-pass digitally filtered at

5 Hz, with a 2.5-Hz transition gap, giving filtering com-

parable to previous data [8]. Swallowing data were nor-

malised to the activity recorded during a maximum

voluntary contraction (MVC) of the same muscle group

[13]. After a short practice period to reduce the risk of

fatigue, the participants were instructed to perform three

MVC manoeuvres [20]:

1. Orbicularis oris: Maximal compression of the upper

and lower lips together

2. Masseter: Maximal teeth clenching

3. Submental and infrahyoid muscle groups: The partic-

ipant’s jaw was held closed firmly by the researcher

and the participant was asked to attempt to open their

jaw against this resistance.

Participants were then asked to complete six swallow

trials, each consisting of 5 ml of water administered via a

teaspoon, with a rest of approximately 10 s between

boluses. To reduce the risk of participants altering their

behaviour because of an awareness of being assessed (i.e.,

increasing volitional effort to swallow ‘‘better’’), the pur-

pose of the study was reinforced to the participants before

the swallow trials, i.e., examination of the assessment

capabilities of the equipment, not the individual’s swal-

lowing ability. For each trial, the participant was instructed

to ‘‘Swallow this in your usual way’’ in order to encourage

the participant to swallow normally.

Measurements

For each bolus, the sEMG graphic trace from the first

swallow elicited was examined for patterns, and measure-

ments were made of peak sEMG amplitude, duration of

sEMG activity, and relative onset of the sEMG activity

among the four muscle groups. Offline analysis of sEMG

data was done to avoid observer bias using Spike 2, with a

specific, dedicated software programme ‘‘Swallow EMG,’’

written by CED. To measure resting baseline activity,

vertical cursors were placed 1 s apart prior to the onset of

an MVC manoeuvre or swallow attempt. The software

calculated the mean ± 2 SD. ‘‘Onset’’ of the swallow was

defined as the point where baseline activity increased into a

swallow pattern, which was defined as the point at which

the EMG trace exceeded 2 SD above baseline for that

channel [19, 21]. If multiple peaks occurred above base-

line, measurements were made of the largest peak that

corresponded temporally with those in the other muscle

groups. The end of swallow activity was determined as the

point when the EMG trace returned to within 2 SD of

baseline levels. Mean durations were taken for each muscle

in each participant. To establish the pattern of muscle

activation, the mean onset of the muscle groups was

measured relative to the onset of the submental group,

which was designated as time 0. The submental muscle

group was chosen as it had been shown to produce reliable

sEMG activity during swallowing, which is associated with

hyoid elevation [7, 8]. Peak amplitudes for each muscle

group for each swallow and MVC were recorded and the

mean baseline was subtracted to control for differing levels

of noise and background electromyographic activity.

190 S. K. Archer et al.: Dysphagia in Duchenne Muscular Dystrophy Assessed Objectively

123

Data Analysis

Means and standard deviations (SD) were calculated across

each participant’s six swallows, and amplitude data were

normalised by conversion into a percentage of the mean

peak MVC for that muscle group. Intrasubject variation for

each measure was examined by comparing the SDs across

each individual’s six swallows. Medians and interquartile

ranges (IQR) of duration and normalised amplitude data

were compared between groups and analysed with the

Kruskal-Wallis test. The Mann-Whitney test was con-

ducted post hoc, adjusting for multiple testing by using the

Bonferroni Correction [22]. Means and SDs of the relative

timing of onset of activity were compared between groups

and analysed with the analysis of variance. Both Excel for

Windows Vista (Microsoft Corp., Redmond, WA, USA)

and the Statistical Package for the Social Sciences (SPSS

v16; SPSS, Inc., Chicago, IL, USA)) were used to perform

the statistical analysis of the data.

Reliability

Three healthy control participants were randomly selected,

using the Research Randomizer programme (http://www.resea

rchrandomizer.org), to repeat the sEMG procedure in order to

examine the reproducibility of the results. Due to the small

sample size, differences between the raw data were examined

descriptively, examining mean differences and SD between

the first and second tests. The results for the different muscle

groups were combined for each measure of reliability.

Results

Thirty-two patients met the inclusion criteria: 15 with

dysphagia, of whom nine were recruited to Group 1 (five

declined to take part and one died before his scheduled

appointment); 17 had intact swallow function, of whom six

were recruited to Group 2, and 11 declined to take part.

Twelve healthy participants formed the control group

(Group 3). Group 3 was significantly older than Group 2

(p = 0.03, Table 1). All DMD participants were wheel-

chair users and dependent for all activities of daily living,

including feeding. One participant in Group 2 had a tra-

cheostomy in situ. Group 1 had a significantly lower FOIS

score than both Group 2 and Group 3 participants

(p B 0.001) (Table 1). Two participants in Group 1 had a

percutaneous endoscopic gastrostomy (PEG) tube in situ to

meet their nutrition and hydration needs. Eight participants

in Group 1 were receiving a modified diet (pureed food)

due to dysphagia. The remaining participant in Group 1

was receiving only teaspoons of fluid by mouth and

otherwise was PEG fed. No participants in Group 2 had any

modifications to their diet. No participants in Group 3 had

any history of dysphagia or neurological or gastrointestinal

disease as determined by face-to-face interview.

The sEMG procedure was well tolerated by all partici-

pants and simple to administer, taking less than 10 min to

complete. The technique consistently produced electro-

myographic signals from which objective measurements of

swallowing activity were made. It was not possible to place

a preamplifier in the infrahyoid muscle position in one

participant in Group 1 due to flexed neck posture, and in

the orbicularis oris muscle site on another participant in

Group 1 due to reported skin sensitivity. Therefore, the

results for these muscle groups in Group 1 are based on

eight participants. It was not possible to measure an

infrahyoid muscle MVC in two of the healthy control

participants as activity was not elicited in this muscle group

during the MVC manoeuvre; therefore, the infrahyoid

amplitude measurements for Group 3 are based on ten

participants.

Examination of the sEMG Trace

Representative sEMG swallow waveforms from individu-

als in each group are shown in Fig. 1. All healthy controls

(Group 3) demonstrated clear, easily identifiable, and

measurable peaks of activity during swallowing in each

muscle group, and then activity returned to baseline levels

(Fig. 1a). In contrast, swallow waveforms from participants

in Groups 1 and 2 showed multiple peaks of activity per

swallow (Fig. 1b, c). In addition, activity was prolonged,

and there was evidence of continued activity after the

swallow, without a return to baseline.

Peak Amplitude

Figure 2 and Table 1 show peak-normalised sEMG ampli-

tude during swallowing for each muscle group. Normalised

peak amplitude was significantly higher in Group 1 than in

Group 3 for orbicularis oris and masseter muscles (p = 0.03

and p \ 0.01, respectively, Table 1). Normalised peak

amplitude was also higher for Group 2 than for Group 3 in

these muscle groups, but this did not reach significance. A

similar nonsignificant trend was observed in the infrahyoid

muscle group (p = 0.15). Peak sEMG activity was signifi-

cantly higher in Group 3 than in Group 2 for the submental

muscle group (p = 0.03, Table 1). There were no other

significant between-group differences.

Duration of Activity

There were no differences between the participant groups

with respect to duration of activity and no clear pattern was

observed (Table 1).


123

http://www.researchrandomizer.org

http://www.researchrandomizer.org

Relative Timing of Activity

The mean order of onset of activity was statistically similar

for all groups: orbicularis oris first, then submental, mas-

seter, and finally infrahyoid (Fig. 3).

Intrasubject Variation

There was significantly higher intrasubject variability in

peak masseter activity in Group 1 than in Group 2

(16.01 % MVC [IQR = 12.82–38.85] vs. 5.86 % MVC

[IQR = 3.58–6.83]; p = 0.02) and in Group 1 than in

Group 3 (16.01 % MVC [IQR = 12.82–38.85] vs. 2.18 %

MVC [IQR = 0.77–6.06]; p =0.02). The difference between

Groups 2 and 3 was not significant. The same trend was

seen for peak amplitude of orbicularis oris and infrahyoid

muscles, with increased variability in the DMD groups and

Group 1 having the most variability, although this did not

reach significance. There were no significant differences

and no trends seen in relative intrasubject variability for

any of the other sEMG measures.

Reliability

The mean differences between the repeated sEMG

assessments were amplitude: 29.12 ± 21.69 % MVC,

duration: 0.69 ± 0.62 s, and relative timing: 0.40 ±

0.24 s.

Discussion

The present study is the first to investigate the clinical

application of sEMG for the assessment of swallowing in

patients with DMD. The technique was well tolerated and

easy to administer, confirming its potential for repeated

objective physiological assessment in patients with pro-

gressive neuromuscular diseases. Of the four muscle

groups tested, there were distinct differences in normalised

peak activity during swallowing between the DMD par-

ticipants with dysphagia, those with preserved muscle

function, and healthy controls. Although there were no

differences in the timing or duration of muscle activity

between the groups, these comparative data provide insight

into the relative activity of orbicularis oris, masseter,

infrahyoid, and submental muscles during swallowing.

Muscle Activation During Swallowing

Dysphagic DMD participants produced greater normalised

peak orbicularis oris and masseter muscle activity during

swallowing, which supports the original study hypothesis.

In healthy subjects, the force produced during swallowing

is only a small percentage of that which can be generated

voluntarily [23]. The dysphagic DMD participants exerted

a relatively higher proportion of maximal activity, i.e., they

were working harder to swallow than the other participant

groups, indicating that they have weaker muscles with less

Table 1 Demographics and

sEMG measurements during

swallowing in the three

participant groups

Data are presented as mean and

[SD] for age and relative timing

of sEMG activity, and as

median and [IQR] for FOIS and

peak and duration of sEMG

activity

* p B 0.05; ** p B 0.01;

*** p B 0.001a Significant difference

between Groups 1 and 2b Significant difference

between Groups 2 and 3c Significant difference

between Groups 1 and 3

Group 1 Group 2 Group 3

(dysphagic DMD

participants)

(nondysphagic

DMD participants)

(healthy controls)

n 9 6 12

Age (years) 21.7 [4.2] 21.0 [3.0]b* 24.8 [3.1]

FOIS 5 [5–5]a*** 7 [7–7] 7 [7–7]c***

Peak sEMG activity (%MVC)

Orbicularis oris 71.87 [49.89–109.82] 58.79 [47.39–66.86] 26.22c* [14.22–52.33]

Masseter 61.77 [25.95–103.50] 19.34 [11.06–36.86] 5.07c** [4.28–13.03]

Submental 25.14 [17.74–86.71] 20.21 [16.09–21.22] 73.46c* [32.68–94.12]

Infrahyoid 80.08 [31.08–91.19] 43.54 [32.94–90.07] 17.71 [9.95–38.22]

Duration of sEMG activity (s)

Orbicularis oris 2.62 [0.55–3.87] 1.89 [1.49–2.25] 1.89 [0.98–2.40]

Masseter 0.29 [0.18–0.54] 0.78 [0.58–1.15] 0.78 [0.55–0.99]

Submental 0.52 [0.36–1.06] 0.95 [0.66–2.31] 1.29 [1.13–1.52]

Infrahyoid 0.45 [0.24–0.76] 0.31 [0.12–0.62] 0.79 [0.70–0.92]

Timing of activity onset relative to submental activity (s)

Orbicularis oris –0.74 [0.85] –0.52 [0.44] –0.71 [0.55]

Masseter 0.09 [0.23] 0.36 [0.53] 0.24 [0.28]

Submental 0 [0] 0 [0] 0 [0]

Infrahyoid 0.16 [0.55] 0.38 [0.47] 0.35 [0.26]


123

Fig. 1 Rectified and smoothed sEMG swallow trace by a participant

from each group, with all muscle groups represented. a Healthy

control participant (Group 3). b Dysphagic DMD participant (Group

1). c Nondysphagic DMD participant (Group 2). Dashed line, peak

swallow activity; dotted line, baseline activity ?2 standard deviations

(2 SD). A, onset of swallow activity; B, offset of swallow activity


123

functional reserve [23]. This finding is consistent with

previous electromyographic studies of myopathic limb

muscles and is indicative of reduced electromechanical

efficiency, with more motor units activated to give the

same force due to loss of muscle fibres [14]. In contrast, the

submental muscle group followed a different activity pat-

tern, with healthy controls producing a significantly greater

percentage of their MVC during swallowing than nondys-

phagic DMD patients. This could be explained by the

difficulty in performing a MVC of these muscles. By using

a nonswallow task for the MVC (resisted jaw opening),

activation of muscles not normally involved in swallowing

was likely (e.g., platysma) and would have been recorded.

Instructing participants to produce a forceful swallow with

maximum effort may have been a more appropriate tech-

nique to produce the maximum activity of the target

muscles.

Dysphagic DMD participants generally had more vari-

ability in activity between swallows than the other groups

and this was significant in the masseter muscles. It is

suggested that this provides further evidence of muscle

weakness and recruitment of multiple motor units during

swallowing in dysphagic DMD patients. The present study

required participants to swallow six successive teaspoons

of water, which arguably is not a demanding task;

therefore, a further study should be conducted in which

participants swallow larger amounts and/or different tex-

tured boluses which might put greater demands on the

swallowing system, potentially leading to increased dif-

ferences between these groups.

Timing of Activation

The results of the present study indicate that DMD does not

consistently affect timing of muscle activation during

swallowing, which is contrary to the results of Crary et al.

[19] who found significantly shorter activity duration in

sEMG assessments of dysphagic stroke patients, and which

suggests that different disease processes exert different

effects on swallowing, as might be expected. A reduction

in duration of activity was predicted a priori in the dys-

phagic patients as a sign of myopathic changes, reflecting a

shortening in motor unit action potentials from a loss of

fibres [16]. However, this was not found, which may reflect

the recorded sEMG signal being a superimposition of all

active motor units during muscle contraction and therefore

not being sensitive to changes in individual motor units.

There was a consistent pattern of onset of muscle group

activity during swallowing in the present study, which was

preserved in DMD participants with dysphagia. The same

Fig. 1 continued


123

sequence of activity in swallowing has been reported pre-

viously [24] and can be related to the order of biomechanical

events in the swallow. The orbicularis oris muscles are

activated first, corresponding to the oral phase of the swal-

low, where the lips are closed to contain the bolus in the oral

cavity [25]. The submental group then elevates the larynx

and may have a role in propulsion of the bolus into the

pharynx [9]. The masseter muscle then activates and stabi-

lises the jaw in the intercuspal position for the onset of

swallowing [26], assisting in the development and mainte-

nance of intraoral pressure to facilitate bolus propulsion.

Finally, the infrahyoid muscles pull the hyoid and attached

larynx downward [27]. The return of the hyoid to the resting

position is a marker of the end of the oropharyngeal swallow

[28]. For all patients and healthy participants, there was an

overlap in the activity for all muscle groups, consistent with

the dynamic nature and overlap of the oral and pharyngeal

components of swallowing.

Examination of the sEMG Trace

All DMD participants, regardless of swallowing status,

produced different patterns on the sEMG trace during

swallowing compared to healthy participants, who pro-

duced clear, easily identifiable single peaks in all muscle

groups as previously reported for healthy subjects [8].

DMD participants had more variable patterns with

numerous and less distinct sEMG peaks, which has also

previously been reported in dysphagic stroke patients [19].

Polyphasic waves on EMG have been reported as a feature

of myopathy, related to loss of muscle fibres within the

motor unit, with recruitment of a greater number of motor

units to compensate for weakness [15]. The baseline sEMG

activity was greater in the DMD participants as also

reported in stroke patients [19]. In DMD, spontaneous

activity, with multiple peaks, complex repetitive dis-

charges, and fibrillation potentials, is well reported in EMG

studies of limb muscles [29] but has not been previously

described in the swallowing muscles.

Despite the marked differences between patients and

healthy controls, there were no consistent pattern differ-

ences in the sEMG trace between the DMD participants

with dysphagia and those with preserved swallow function.

While the nondysphagic patients were not showing clinical

signs of swallowing impairment, the sEMG findings indi-

cate that there were physiological changes to their swal-

lowing muscles. This is consistent with previous data from

oligosymptomatic patients with DMD who showed myo-

pathic changes on needle EMG studies of limb muscles

[15]. This finding may be indicative of the continuum of

disease, which is a particular consideration with recruit-

ment of participants at the more severe end of the disease

spectrum in the present study (from an adult respiratory

clinic). Crary et al. [8] found that observers could reliably

and accurately identify normal swallows from nonswallow

activity in sEMG traces. However, it remains to be deter-

mined whether it is possible to discriminate between nor-

mal and abnormal swallows from their sEMG trace with a

similar level of accuracy.

Reliability

The descriptive test–retest assessment in the present study

was based on a very small sample of healthy partici-

pants and the reproducibility in the patient population

remains unknown. Nonetheless, the mean differences in

Fig. 2 Peak sEMG amplitude

during swallowing for each

muscle group across participant

groups. Group 1, dysphagic

DMD participants; Group 2,

nondysphagic DMD

participants; Group 3, healthy

controls. Medians and

interquartile ranges are

presented, compared with the

Mann-Whitney U test and

corrected for multiple testing

with the Bonferroni Correction.

*p \ 0.05; **p \ 0.01


123

measurements across the repeated sEMG assessments in

the present study highlight the need to examine further the

reliability of sEMG before it is used in clinical assessment.

The sEMG signal can be influenced by many factors, which

may be physiological, experimental, or technical and are

likely to affect reproducibility [30]. These influences may

be particularly difficult to control for when using sEMG to

assess muscle activity in swallowing, which is a highly

complex, adaptive motor activity [21]. However, some

authors are already using sEMG to assess swallow function

[10, 31] before arguably necessary research has been

completed.

Critique of the Method

A limitation of this study was the small sample size and the

considerable refusal rate, although no differences were

noted from the medical notes between those who declined

to take part and those who participated, and the patients

were recruited from a tertiary referral centre, enabling

relatively good access to a rare patient population. This

study was necessarily exploratory as no similar work has

been conducted previously, and we believe that this

detailed physiological pilot study has provided the data and

justification to power a larger clinical study to determine

the role of sEMG as a simple, objective, physiological

biomarker for dysphagia. In addition, we appreciate that

the method of classification of DMD participants into

dysphagic and nondysphagic groups could be questioned as

it was based on a diagnosis of dysphagia made by a speech

and language therapist or on a statement of normal swal-

lowing made by a physician, rather than on an instrumental

swallowing assessment. However, all of the patients were

recruited from a specialist centre, with one Specialist SLT

and two experienced consultants in the established team,

all of whom were experienced in assessing swallow func-

tion, and a validated scale (the FOIS) was used to classify

impairment. The healthy control group was older than the

nondysphagic DMD participants, but the difference was

small and there is no reported change in swallowing

function in the healthy population until advanced age [20].

Differences in muscle activity during swallowing

between the groups could be influenced by differences in

intentional effort, i.e., dysphagic patients may have been

actively trying to swallow ‘‘better.’’ However, to control

for this, all participants were given the same instructions

which were aimed to encourage their normal swallowing

behaviour. It is therefore felt that the increase in activity in

the dysphagic patient group is more likely to reflect muscle

weakness. A limitation of sEMG is that all muscles

involved in swallowing cannot be examined, and sEMG

cannot be used to specifically measure lingual strength,

which is important in bolus propulsion [32]. However,

activity of the lingual muscle has been shown to contribute

significantly to the collective signal measured from the

submental region, which was recorded [33], and a strength

of this study was the examination of four different oral and

pharyngeal muscle groups that all contribute to swallow-

ing. Furthermore, the ability of sEMG to detect a repre-

sentative, composite signal of the activity of the underlying

muscle group [30] means it arguably lends itself to the

assessment of swallowing, which incorporates activation of

many muscles.

An accepted method was used for determining onset and

offset of activity, in which baseline ? 2 standard devia-

tions was considered the threshold [19, 21]. However, with

the multiple peaks and activity after the swallow observed

in the patient groups, this method became less reliable.

Fig. 3 Timing of onset of

muscle group activity relative to

submental activity during the

swallow. The three participant

groups are shown. Group 1,

dysphagic DMD participants;

Group 2, nondysphagic DMD

participants; Group 3, healthy

controls. The symbols represent

means and the lines represent

95 % confidence intervals


123

While a consistent method for peak identification was used,

it increased the subjective element of the analysis. Further

studies examining the sEMG trace with simultaneous direct

visualisation of the swallow with either FEES or video-

fluoroscopy would enable identification of sEMG mea-

surements that are most clinically meaningful.

Conclusion

This is the first investigation of the clinical usefulness of

sEMG for the assessment of swallowing function in

patients with DMD. The technique was well tolerated and

quick to administer, enabling easy and objective recording

of data. Compared to controls, dysphagic DMD patients

produced a greater proportion of their maximum voluntary

muscle activity when swallowing, indicating muscle

weakness. Furthermore, characteristic differences were

present in the pattern of activity during swallowing

between DMD patients and healthy controls, indicative of

myopathic changes in the muscle groups tested. However,

distinct differences between DMD patients with dysphagia

and those DMD patients with intact swallow function were

not found, indicating that there are subclinical physiolog-

ical changes to the muscles for swallowing in DMD, which

is consistent with previous studies of limb muscles. While

this finding limits the value of the sEMG technique for

diagnosing dysphagia in DMD, this study has shown that

sEMG provides useful physiological information about

changes to swallowing muscles in DMD, justifying further

study.

Acknowledgments This work was performed as part of a MRes in

Biomedical Sciences at St George’s, University of London. The

authors acknowledge with gratitude the help given by Mr. David

Crick at Cambridge Electronic Design (Cambridge) who wrote the

script ‘‘Swallow EMG’’ for the Spike 2 data analysis programme. The

authors acknowledge the help given by Prof. Di Newham from King’s

College London in reviewing the manuscript. The authors acknowl-

edge financial support from the Department of Health via the National

Institute for Health Research (NIHR) comprehensive Biomedical

Research Centre award to Guy’s & St Thomas’ NHS Foundation

Trust in partnership with King’s College London and King’s College

Hospital NHS Foundation Trust.

Conflict of Interest The authors report no conflicts of interest

concerning the materials or methods used in this study or the findings

reported in this paper.

References

1. Manzur AY, Muntoni F. Diagnosis and new treatments in mus-

cular dystrophies. J Neurol Neurosurg Psychiatry. 2009;80(7):

706–14.

2. Hill M, Hughes T, Milford C. Treatment for swallowing diffi-

culties (dysphagia) in chronic muscle disease. Cochrane Database

Syst Rev. 2004;2:CD004303.

3. Shinonaga C, Fukuda M, Suzuki Y, Higaki T, Ishida Y, Ishii E,

Hyodo M, Morimoto T, Sano N. Evaluation of swallowing

function in Duchenne muscular dystrophy. Dev Med Child

Neurol. 2008;50(6):478–80.

4. Nozaki S, Umaki Y, Sugishita S, Tatara K, Adachi K, Shinno S.

Videofluorographic assessment of swallowing function in patients

with Duchenne muscular dystrophy. Clin Neurol. 2007;47(7):407–12.

5. Hanayama K, Liu M, Higuchi Y, Fujiwara T, Tsuji T, Hase K,

Ishihara T. Dysphagia in patients with Duchenne muscular dys-

trophy evaluated with a questionnaire and videofluorography.

Disabil Rehabil. 2008;30(7):517–22.

6. Aloysius A, Born P, Kinali M, Davis T, Pane M, Mercuri E.

Swallowing difficulties in Duchenne muscular dystrophy: Indi-

cations for feeding assessment and outcome of videofluoroscopic

swallow studies. Dysphagia. 2009;24(1):123–4.

7. Crary MA, Carnaby GD, Groher ME. Biomechanical correlates

of surface electromyography signals obtained during swallowing

by healthy adults. J Speech Lang Hear Res. 2006;49(1):186–93.

8. Crary MA, Carnaby GD, Groher ME. Identification of swallow-

ing events from sEMG signals obtained from healthy adults.

Dysphagia. 2007;22(2):94–9.

9. Palmer PM, Luschei ES, Jaffe D, McCulloch TM. Contributions

of individual muscles to the submental surface electromyogram

during swallowing. J Speech Lang Hear Res. 1999;42(6):

1378–91.

10. Vaiman M. Standardization of surface electromyography utilized

to evaluate patients with dysphagia. Head Face Med. 2007;3:26.

11. Vaiman M, Eviatar E, Segal S. Surface electromyographic studies

of swallowing in normal subjects: A review of 440 adults. Report

3. Qualitative data. Otolaryngol Head Neck Surg. 2004;131(6):

977–85.

12. O’Kane L, Groher ME, Silva K, Osborn L. Normal muscular

activity during swallowing as measured by surface electromy-

ography. Ann Otol Rhinol Laryngol. 2010;119(6):398–401.

13. Armijo-Olivo S, Gadotti I, Kornerup M, Lagravere MO, Flores-

Mir C. Quality of reporting masticatory muscle electromyogra-

phy in 2004: a systematic review. J Oral Rehabil. 2007;34(6):

397–405.

14. Liguori R, Fuglsang-Frederiksen A, Nix W, Fawcett P, Andersen

K. Electromyography in myopathy. Clin Neurophysiol. 1997;

27:200–3.

15. Emeryk-Szajewska B, Kopec J. Electromyographic pattern in

Duchenne and Becker muscular dystrophy. Part I. Electromyo-

graphic pattern in subsequent stages of muscle lesion in Duchenne

muscular dystrophy. Electromyogr Clin Neurophysiol. 2008;

48:265–77.

16. Fuglsang-Frederiksen A. The role of different EMG methods in

evaluating myopathy. Clin Neurophysiol. 2006;117:1173–89.

17. Crary MA, Carnaby MGD, Groher ME. Initial psychometric

assessment of a functional oral intake scale for dysphagia in

stroke patients. Arch Phys Med Rehabil. 2005;86(8):1516–20.

18. Johnson SW, Lynn PA, Miller JSG, Reed GA. Miniature skin-

mounted preamplifier for measurement of surface electromyo-

graphic potentials. Med Biol Eng Comput. 1997;15:710–1.

19. Crary MA, Baldwin BO. Surface electromyographic character-

istics of swallowing in dysphagia secondary to brainstem stroke.

Dysphagia. 1997;12(4):180–7.

20. O’Dwyer NJ. Control of speech muscles in normal and cerebral-

palsied speakers: an electromyographic analysis. Kensington:

University of New South Wales; 1988.

21. Ding R, Larson CR, Logemann JA, Rademaker AW. Surface

electromyographic and electroglottographic studies in normal


123

subjects under two swallow conditions: normal and during the

Mendelsohn manuever. Dysphagia. 2002;17(1):1–12.

22. Bland JM, Altman DG. Multiple significance tests: the Bonfer-

roni method. BMJ. 1995;310:170.

23. Burkhead LM, Sapienza CM, Rosenbek JC. Strength-training

exercise in dysphagia rehabilitation: principles, procedures, and

directions for future research. Dysphagia. 2007;22:251–65.

24. Ono T, Iwata H, Hori K, Tamine K, Kondoh J, Hamanaka S,

Maeda Y. Evaluation of tongue-, jaw-, and swallowing-related

muscle coordination during voluntarily triggered swallowing. Int

J Prosthodont. 2009;22(5):493–8.

25. Logemann JA. Swallowing disorders. Baillieres Best Pract Res

Clin Gastroenterol. 2007;21:563–73.

26. Monaco A, Cattaneo R, Spadaro A, Giannoni M. Surface elec-

tromyography pattern of human swallowing. BMC Oral Health.

2008;8:6.

27. Humbert IA, Poletto CJ, Saxon KG, Kearney PR, Crujido L,

Wright-Harp W, Payne J, Jeffries N, Sonies BC, Ludlow CL. The

effect of surface electrical stimulation on hyolaryngeal movement

in normal individuals at rest and during swallowing. J Appl

Physiol. 2006;101:1657–63.

28. Martin-Harris B, Michel Y, Castell DO. Physiologic model of

oropharyngeal swallowing revisited. Otolaryngol Head Neck

Surg. 2005;133:234–40.

29. Eeg-Olofsson KE. Dystrophinopathies. In: Stalberg E, editor.

Clinical neurophysiology of disorders of muscle and neuromus-

cular junction. Amsterdam: Elsevier; 2003. p. 429–41.

30. Hogrel JY. Clinical applications of surface electromyography

in neuromuscular disorders. Neurophysiol Clin. 2005;35(2–3):

59–71.

31. Vaiman M. Surface electromyography in preoperative evaluation

and postoperative monitoring of Zenker’s diverticulum. Dys-

phagia. 2006;21(1):14–20.

32. Kennedy D, Kieser J, Bolter C, Swain M, Singh B, Waddell JN.

Tongue pressure patterns during water swallowing. Dysphagia.

2010;25:11–9.

33. Huckabee ML, Steele CM. An analysis of lingual contribution to

submental surface electromyographic measures and pharyngeal

pressure during effortful swallow. Arch Phys Med Rehabil.

2006;87(8):1067–72.

Sally K. Archer MRes, BMedSci (Hons), MRCSLT

Rachel Garrod PhD, MSC, MCSP

Nicholas Hart MBBS, BSc, MRCP, PhD

Simon Miller PhD


123

Dysphagia in Duchenne Muscular Dystrophy Assessed Objectively by Surface Electromyography

Documents

Transcript of Dysphagia in Duchenne Muscular Dystrophy Assessed Objectively by Surface Electromyography