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Neurology of swallowing

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 Journal of Electromyography and Kinesiology 23 (2013) 619626

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Journal of Electromyography and Kinesiology

journal homepage: www.elsevier.com/locate/jelekin

An electrophysiological study of the sequential water swallowing

N. Grgr a,, S . Arc a, Tlay Kurt Incesu a, Y. Seil a, F. Tokuoglu a, C. Ertekin b
a
Atatrk Research and Training Hospital Department of Neurology, Yesilyurt, Izmir, Turkey
b
Ege University, Medical School Hospital, Department of Neurology, Turkey1

a r t i c l e i n f o a b s t r a c t

Article history: Background: Sequential water swallowing (SWS) was mostly investigated by the videouoroscopic and
Received 10 August 2012 endoscopic methods. However some physiological features of SWS was rarely evaluated by neurophysi-
Received in revised form 21 December 2012 ological techniques. Our aim was to investigate some neural and muscular changes on sequences of SWS
Accepted 21 December 2012
using electromyography (EMG) methods.
Methods: Fifty-eight normal adults were investigated. SWS was initiated voluntarily with 50 ml and
100 ml water volumes from a cup. Submental EMG, respiratory signals, heart rate, and sympathetic skin
Keywords:
Sequential water swallowing
responses (SSR) were measured during SWS.
Respiration Key results: All parameters were increased signicantly during the 100 ml SWS. During swallowing apnea
Aging period, compensatory respiration cycles occurred in 24% and 48% of participants in the 50 ml and 100 ml
Dysphagia SWS, respectively. Heart rate increased during swallowing apnea. SSR were evoked just before and just
Heart rate after the SWS in more than halves of participants. A foreburst EMG in SM muscles at the initiation of
Sympathetic skin responses SWS was recorded in 86% of normal participants. Older age was associated with a prolonged duration
Swallowing apnea of the apnea period.
Conclusions: All parameters of the SWS could be recorded numerically and objectively using electrphys-
iological methods. These are similar to those obtained by videouoroscopic and similar methods. The
foreburst activity of the initiation of SWS may represents preparatory activity from the activation of
the fast cortical descending motor pathway. Increasing heart rate and the prolonged apnea urged that
older people and patients could be carefully tested for respiratory and cardiac rhythm disorders.
2012 Elsevier Ltd. All rights reserved.

1. Introduction
Continuous sequential cup/straw swallowing or sequential
water swallowing (SWS) in humans has recently been recognized
as a more logical approach to evaluate the physiology of degluti-
tion and to diagnosis dysphagia (Chi-Fishman and Sonies, 2000;
Daniels et al., 2004; Daniels and Foundas, 2001). SWS is a common
daily occurrence characterized by multiple, successive, rapid swal-
lows (Chi-Fishman and Sonies, 2000; Lederle et al., 2011).
During SWS, there are rhythmic or pseudorhythmic swallow se-
quences without pause, as SWS requires breath-holding resulting
in a swallowing apnea period. However, SWS may have longer
interswallow intervals especially at the end of last swallows; this
is compensated for by the inspiration/expiration respiratory cycle
(Daniels et al., 2004) Breathing can also be interspersed between
swallows at the midpoint of SWS even in normal subjects (Chi-
Fishman and Sonies, 2000; Chi-Fishman et al., 1998; Cruccu
Corresponding author.
E-mail addresses: nevin.gurgor@gmail.com, nevin@dr.com (N. Grgr), cumhur-
ertekin@gmail.com (C. Ertekin).
1
Retired.
et al., 1990). It should be expected that after the rst swallow in
SWS, subsequent swallows could be primarily initiated at the
hypopharynx in normal subjects; these would be most prone to
produce laryngeal penetration (Daniels et al., 2004; Daniels and
Foundas, 2001).
When the water volume is increased for SWS, laryngeal pene-
tration or aspiration frequently occurs (Dosier et al., 2006; Lederle
et al., 2011; Martin et al., 1994) There are also reports of an effect
of aging on SWS with laryngeal penetration occurring more fre-
quently in older adults (Daniels et al., 2004; Mcculloch et al., 2007).
Most studies of SWS in normal humans have used videouoros-
copy or similar techniques. However, the relationship between res-
piration and swallowing and other physiological events during
SWS has never rarely studied by electrophysiological methods.
In this study we applied electrophysiological methods to evalu-
ate along with SWS and to try some relation with central nervous
system. We proposed that the onset of SWS is induced by volun-
tary control while subsequent swallows and other autonomic
and respiratory activity are somewhat related either by the swal-
lowing induced factors circulating at the brainstem; or the result
of central nervous activities; or both.

1050-6411/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jelekin.2012.12.003
620 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626
2. Materials and methods
Fifty-eight normal healthy adults without any swallowing com-
plaints were investigated (21 male, 37 female) exclusion criteria
were muscle, nerve and brain disorders; mean age was 48.4 years
(range, 2083 years). All participants were voluntary and included
hospital staff and patients relatives. The ethics committee of our
hospital approved the study and all participants provided informed
consent. During the examination, the seated participant was in-
structed to hold their head in neutral upright position. All examin-
ations were performed in the afternoon at least 2 h after lunch.
In order to understand the aging effects on SWS, we divided
part of participants into two groups. The young group had the
mean age of 31.8 years (range, 2039 years) and included 17 par-
ticipants (10 female, 7 male). The older group had a mean age of
69.2 years (range, 6083 years) and included 14 participants (9 fe-
male, 5 male).
2.1. Sequential water swallowing (SWS)
Liquid swallows of tap water were initiated voluntarily with 50
and 100 ml water in a disposable cup positioned in between the
lips before the any command was given. Water temperature was
approximately 2325 C. Swallowing signals were recorded from
submental/suprahyoid EMG. The submental EMG (SM-EMG) was
recorded using bilateral silversilver chloride (AgAgCl) EEG elec-
trodes taped under the chin over the submental muscle complex
(mylohyoid, geniohyoid, and anterior digastric muscles). The skin
overlying the submental complex was cleaned and the electrogel
(Lome EEG paste) was also used with the EMG surface electrodes
placed for submental recordings. Signals were ltered (band pass
10010 kHz), amplied, rectied, and integrated. Total analysis
time was adjusted to 20 s for each set of SWS.
Baseline EMG activity were initiated for several seconds prior to
onset of SWS; afterward the instruction to swallow was given by
the examiner. Subjects were asked to drink water continuously
as they do in their daily life just before they were asked to start
drinking. The SWS test was repeated three times with 50 and
100 ml water drinking in all subjects. The third SWS traces for each
subjects were selected for the individual measurement. The third
trial was of SWS found to be the most sophisticated and reliable
measurement comparing previous two SWSs. The number of swal-
lows were recorded and counted according to the periodic move-
ments on SM-EMG. Total duration of SWS was calculated from
the onset of the rst EMG burst to the end of the last swallow on
the SM-EMG traces in a SWS epoch. Four channel-EMG apparatus
were used (Nicolet-Viking V.11.0).
2.2. Swallowing apnea measurement during SWS
The swallowing apnea period of respiration was studied in all
participants. For this purpose, an additional EMG channel was used
simultaneously. The respiratory signal was obtained via a nasal
cannula (Sleep Sense) and placed at the entry of the nostrils
and connected to the EMG machine. Airow direction was re-
corded as a negative polarity representative of inspiration and a
positive polarity representative of expiration. The SM-EMG and
phase of respiration were simultaneously recorded to detect swal-
lowing apnea and respiratory phase pattern before, during, and
after 50 or 100 ml of SWS. Respiratory signals were also recorded
at rest. A plateau in the respiratory signal along the baseline indi-
cated an apneic period. EMG lters for the respiratory channel
were adjusted with a band pass of 0.230 Hz.
2.3. Electrocardiogram and heart rate
We simultaneously recorded electrocardiogram (ECG) data in a
third channel of the EMG using silversilver chloride cup elec-
trodes. One of the electrodes was placed on the second left inter-
costal space and a second was placed on the dorsum of the hand.
Hearth rate was measured before and during SWS. ECG signals
were ltered (band pass 0.230 Hz) and amplied.
2.4. Sympathetic skin response (SSR) measurements
The SSR was recorded from the skin of the left hand. The skin
surface was cleaned and silversilver chloride electrodes were
placed on the skin of the palm and dorsum of the hand using elec-
trogel (Lome EEG paste) The low frequency lter was 0.2 Hz and
the high frequency lter was 100 Hz. Spontaneous electrodermal
activity (EDA) or background uctuations of EDA were rst re-
corded for 20 s with the subjects at rest. During the 50 ml and
100 ml SWS tests, the rst SSR was evoked after the examiners
command to swallow. The rst SSR was related to attention
and is called the arousal SSR for the sake of brevity. SSR and heart
rate changes during SWS were evaluated and reviewed in detail
elsewhere.
2.5. Order of experiments
We rst recorded basal respiration and heart rate. Afterwards,
the SWS test was conducted three times with 50 ml water followed
by three times with 100 ml water. There were intervals (1
5 min) between each experiment. If participants needed additional
interval time, this was also permitted in order to create a more re-
laxed environment. His or her head was stabilized by one of the
examiners hand from the top of head during all experiments.
2.6. Statistical methods
The mean and standard deviation (SD) and standard error of
mean (SEM) of all measured quantities were calculated and
paired-t test was applied for comparisons. Chi-square analyses
were used to test for differences in percentage of respiratory pat-
tern between 50 and 100 ml SWS. Signicance was tested at the
0.5% level. Statistical analysis was conducted using the SPSS statis-
tical package.
3. Results
3.1. Effect of bolus volume in SWS
After the command to swallow, normal adult subjects could
perform swallowing movements recorded from SM muscles that
were quite rhythmic (Fig. 1). Table 1 reports swallowing measure-
ments and other parameters. As expected, the number of swallows
and the duration of SWS increased signicantly with 100 ml SWS
(p < 0.0001). This means that when the amount of water is in-
creased, the number of swallows and subsequently the duration
of SWS are proportionally increased. However, there were two
ndings that were not usually expected in normal subjects: the
rst SM-EMG bursts showed some interesting features that can
be called foreburst of SWS. These occurred after the command
of swallow by examiner; however they almost always appeared
just before or during the last respiratory cycles and before swal-
lowing apnea. They were often smaller in amplitude than the sub-
sequent swallow bursts and sometimes longer in duration as
swallowing continued (Figs. 1 and 2). However, the foreburst of
SWS could not be found in 10 of 58 participants; they were seen
 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626 621

Fig. 1. Sequential water swallowing (100 ml). First channel: SM-EMG (The
foreburst is lined). Second channel: respiration (Resp) (nasal cannula). Third
channel: ECG. Fourth channel: electrodermal activity and rst SSR. Note: the
foreburst occurs with the last respiratory cycle, before the apnea interval.

Table 1
Statistical results* of SM-EMG, respiration and heart rate changes after 50 ml and
100 ml water swallowing (SWS). Fig. 2. The initiation of 100 ml SWS. First channel: SM-EMG. Second channel:
respiration (nasal cannula). Third channel: sympathetic skin response (SSR). Note:
50 ml SWS* 100 ml P the typical foreburst and SSR just after instruction from the examiner.
SWS*
1. Number of swallows 4.7 1.3 0.1 6.4 1.6 0.2 <0.0001
37 411 than those of the non-swallowing period. They mostly appeared
2. SWS duration (s) 6.3 2.0 0.2 7.8 2.0 0.2 <0.0001 with long inter-swallow intervals.
310.5 414 We compared participants with and without compensatory res-
3. Swallowing apnea (s) 6.1 1.9 0.2 7.0 2.1 0.2 <0.0003 piration during swallowing apnea during the 50 ml and 100 ml
2.510 312 SWS. In the 50 ml SWS, subjects with compensatory respiration
4. Heart rate (basal)/(min) 76.4 11.6 76.4 11.6 NS during swallowing apnea showed increased number of swallows
1.5 1.5 (p = 0.0004), SWS duration (p = 0.0002), and apnea interval
5. Heart rate (during swallowing 88.4 12.3 88.5 12.2 NS (p = 0.03) compared to participant without compensatory respira-
apnea)/min 1.1 1.6 tion. Results were similar for the 100 ml SWS, although the num-
P < 0.0001** P < 0.0001** ber of swallows and swallowing apnea were not signicantly
*
Mean SD, SEM, Range. different between the two groups. The increase in water volume
**
p Values obtained from the comparison of the basal and SWS conditions for from 50 ml to 100 ml may produce more risk but this was probably
heart rate. compensated by the increase number of extraneous respiratory cy-
cles from 24% to 48%.
Table 1 reports changes in heart rate during SWS. In basal con-
in 86% during the 50 ml SWS. Similarly, the foreburst was found in ditions before swallowing, mean heart rate was 76/min. During
approximately 86% of participants during the 100 ml SWS. Thus swallowing (either 50 or 100 ml SWS), heart rate was increased
there is no difference in the appearance of a foreburst of SWS to approximately 88 beats/min (p = 0.001) (Fig. 4). This is the
in 50 ml versus 100 ml SWS (Table 2). well-known swallowing tachycardia described more than a cen-
A second important observation during SWS is that there were tury ago by Meltzer (Sheroziya et al., 2003). All heart rate changes
compensatory respiration cycles (inspiration/expiration) during occurred during the apnea interval. After the apnea interval the
the swallowing apnea period while participants were sequentially heart rate dropped to basal values. Arousal SSR could be evoked
swallowing (Fig. 3). During the 50 ml SWS, 14 participants demon- in approximately 52% of participants; at the end of SWS, second
strated such compensatory respiratory cycles within the swallow- SSR was found in nearly the same number of cases.
ing apnea period (approximately 24%). However, during the 100 ml
SWS the compensatory respiratory cycles were signicantly more 3.2. Age effects on SWS
common, being found in 28 subjects (approximately 48%). It was
not uncommon to observe the compensatory respiratory cycle be- Table 3 and Fig. 5 shows the effect of age on SWS values. There
tween the last interswallow interval of SWS. Indeed the last swal- were no signicant differences between the two age groups with
lows during SWS had slightly longer intervals compared to the rst the exception of swallowing apnea, which was prolonged in the
swallows (Fig. 3). However, the compensatory respiration could older age group on the 50 ml SWS (p < 0.042) (Fig. 5). Although
also be recorded in the midst of SWS during swallowing apnea. the mean duration of the 50 and 100 ml SWS were increased in
The most striking feature of the respiratory cycles or compensatory the older age group, this did not reach statistical signicance.
respiration was found during the inter swallow intervals. A second The rate of compensatory respiratory cycles was similar be-
feature was that the onset was mostly inspiration and immediately tween age groups. In the 50 ml SWS, 29% of both groups showed
continued with expiration. Their amplitudes were often higher compensatory respiration cycles. In the 100 ml SWS, 47% and
622 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626

Table 2
Electrophysiological features of the foreburst activity in 50 ml and 100 ml SWS.

Number of Foreburst activity recorded from Mean Mean _

Interval between the peak of foreburst
cases number of cases M SD SEM amplitde (mV) duration (s) and the peak of rst swallow (s)
50 ml SWS 58 50 (86%) 71.5 34 1.9 0.7 1.5 0.8
4.8 0.1 0.1
100 ml SWS 58 50 (86%) 68.5 26.8 1.8 0.7 1.5 1.4
3.8 0.1 0.2

There were no statistical signicant value in between 50 and 100 ml SWS.

Table 3
Statistical summary of SWS study for young and old normal participant.

Parameters Young Signicants Old

people*n = 17 people*n = 14
Number of swallows 4.7 1.3 (0.3) NS 4.8 1.5 (0.4)
50 ml SWS 37 49
100 ml SWS 6.8 1.6 (0.4) 6.5 1.5 (0.4)
NS
410 49
Duration of swallows (s) 5.9 2.1 (0.5) 6.8 2.6 (0.7)
50 ml SWS 3.010.0 NS 3.010.5
100 ml SWS 7.7 2.0(0.4) 8.6 2.2(0.6)
NS
Fig. 3. Sequential water swallowing (100 ml). First channel: SM-EMG. Second 512 514
channel: respiration and swallowing apnea, Note: compensatory respiratory cycle
Swallowing apnea (s) 5.3 1.9 (0.4) 7.1 2.3 (0.6)
in between last swallows during the apnea period (arrow).
50 ml SWS 2.510 0.042 3.510.5
100 ml SWS 6.9 2.1(0.5) 7.8 2.6(0.6)
NS
411
Heart rate basal/(min) 81 13.6(3.3) NS 74 10.27 (2.8)
50 ml SWS 60111 5793
100 ml SWS 81 13.63(3.3) NS 74 10.27(2.8)

60111 5793
Heart rate apnea/(min) 97.7 11.5(2.8) 83.4 9.6 (2.6)
50 ml SWS 68114 0.001** 68112
100 ml SWS 96.4 14.4(3.5) 0.003** 83.3 8.1(2.2)

60118 68112
Heart rate increase during 15.0 7.6 (1.8) NS 9.5 7.11 (1.9)
SWS apnea 3.033 0.021
50 ml SWS 13.7 6.9(1.6) 8.2 6.2(1.6)
100 ml SWS NS
026 0.021

*
mean SD, SEM, Range.
**
They were compared by the basal values of ECG.

conclude there was again no difference between young and old

participants (Table 4). One variation was that the initiation and
end of swallowing apnea was completed much more frequently
with expiration in the older age group (71.4%) compared to the
younger group (64%).

3.3. Initiation and termination of SWS

Fig. 4. Comparison of ECG between baseline and during swallowing apnea
interval. Each line denotes a case investigated. Vertical line is heart beats per
minute. In the apnea interval, there is clear-cut tachycardia.
50% of young and older participants showed compensatory respira-
tion cycles, respectively. The 50 ml SWS was safer than the 100 ml
SWS irrespective of age. If the expiration or inspiration relationship
resulted in the initiation and termination of swallowing apnea; we
Some specic features were recognized at the initiation of SWS.
As shown in Fig. 2, the examiners order to swallow rst pro-
duced the foreburst on SM-EMG, which was elicited even before
or mostly during the last cycle of respiration in 87% of participants.
During or just after the rst respiration cycle, an arousal SSR was
evoked in approximately 52%. Some participants showed another
SSR just after the end of the sequential swallowing and apnea period,
unrelated to water volume. However, this second SSR was not re-
 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626 623

Fig. 5. Young and older healthy participants, 50 ml SWS with SM-EMG (upper) and respiration (respiration, lower trace). Note: increase of swallowing apnea interval and
compensatory respiratory cycle during the apnea period in older participants.

Table 4 described. The foreburst began immediately after the examiners

The onset and end of SWS apnea. instruction. It does not seem to be a deection of the initial swal-
Young peoples Old peoples n = 14
low. We think this for several reasons. First, the foreburst is lower
n = 17 in amplitude and longer in duration than the subsequent swallow
50 ml SWS
deexions. It is also the rst event in the SWS procedure. It was al-
Expiration/expiration n = 11 64.70% n = 10 71.43% ways formed just before the onset of swallowing apnea. It appears
Expiration/inspiration n=5 29.42% n=4 28.57% within the regular respiratory movements and can even overlap
Inspiration/expiration n=1 5.88% the last respiratory cycle before the swallowing apnea period
Inspiration/inspiration
(Figs. 1 and 2 and Table 2). It is probably either a type of startle re-
100 ml SWS sponse or, more likely, it may present a preparatory EMG signal
Expiration/expiration n=9 52.94% n = 11 78.57%
produced by the descending motor pathway(s) to the suprahyoid
Expiration/inspiration n=6 35.30% n=3 21.43%
Inspiration/expiration n=1 5.88% muscles.
Inspiration/inspiration n=1 5.88% During sequential swallowing, the rst cortical input is thought
to descend to the brainstem neural network or swallowing central
pattern generator (CPG) based on experimental studies (Martin
corded in approximately half of participants (Fig. 6). During termina- and Sesle, 1993; Miller, 1982; Narita et al., 1999). During such a
tion of SWS, the last swallow often showed longer intervals than the voluntarily-induced swallow (Ertekin, 2011), the regions of the
previous interswallow intervals (see Figs. 1 and 3). The interswallow cortex and subcortical areas involved with swallowing serve
interval could be compensated by a respiratory cycle, either expira- mainly to trigger deglutition and to control the beginning of the
tion to inspiration or vice versa. In most participants the swallowing motor sequences, after triggering of SWS and during the sequential
was completed without compensatory respiratory cycles. Swallowing deglutition (Ertekin and Aydogdu, 2003; Jean and Car, 1979; Lang,
tachycardia was particularly apparent during the latter parts of swal- 2009; Nishino, 1993; Thexton et al., 2007). On the other hand, the
lowing apnea. After the end of swallowing, heart rate immediately most consistent cortical activation is seen in the primary motor
decreased to the basal level. (see Figs. 1 and 4). and primary sensory cortices (Hamdy et al., 1999; Martin et al.,
2004; Mossier et al., 1999; Suzuki et al., 2003). It has been demon-
4. Discussion strated that motor planning of voluntary swallow or sensory stim-
ulation of the oropharynx may activate the supplementary motor
SWS can be subdivided into three parts for analysis: initiation, area, insula, cingulated cortex, premotor cortex, basal ganglia,
swallowing apnea period and termination, by means of EMG and cerebellum without any signicant act of swallowing (Abe
methods. et al., 2004; Lowell et al., 2008; Sros et al., 2008). Thus our fore-
burst is an activation related to the preparation of SWS just before
4.1. Initiation of SWS its onset, with a duration of approximately 14 s, similar to reports
mentioned above. When the instruction of the examiner was heard
The initiation of SWS was voluntary. The foreburst of SWS in the fast auditive afferent pathways should be activated to stimu-
one of the most important phenomenon, and it has not yet been late the M1 cortex and cingulated cortex. As a result, the prepara-
624 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626
Fig. 6. Termination of SWS. First channel: SM-EMG. Second channel: respiration (Resp). Third channel: EDA and SSR. Note; compensatory respiration during the apnea
interval (underlined) and the second SSR around the termination of SWS (arrow).
tory SWS can be elicited by means of the very fast cortico-bulbar
pathways with onset latencies of less than 1015 ms to the perio-
ral muscles, as determined by transcranial magnetic stimulation
(TMS)Cruccu et al., 1990; Liscic et al., 1998; Meyer et al., 1994;
Yldz et al., 2005.
It is well known that the SSR can be evoked by any kind of arou-
sal stimuli (Dawson et al., 2000; Vetrugno et al., 2003). In order for
our instruction to produce this kind of arousal, the SSR must be
evoked by cortico-subcortical processes. The onset of arousal SSR
is later than the onset of foreburst but before swallowing apnea.
This may suggest that the arousal SSR could be initiated by the
sound-induced cortico-subcortical mechanisms. The anterior cin-
gulate cortex or thalamo-cortical limbic circuits and lower brain-
stem structures including nucleus tractus solitarii (NTS)were
demonstrated to positively correlate with neural activity in sub-
jects experiencing auditory and arousal stimuli with SSR (Frederik-
sen et al., 1998; Korpelainen et al., 1993; Pron et al., 1995). The
arousal SSR could be evoked in about half of the participants. This
may suggest that they have somewhat different central sources.
Probably, the SSR is related to concentration or attention of partic-
ipants. Fast habitiation may also cause the absence of SSR in some
participants. When the presence of both SSR and foreburst activity
may strongly demonstrated that the initial part of SWS is related
with cortical voluntary preparation process of deglutition.
4.2. The swallowing apnea period
The swallowing apnea period during the 50 ml or 100 ml SWS
can be controlled voluntarily, spontaneously, or both. However,
the last two swallows often had longer inter-swallow interval than
other swallows in the same set, and the longer inter swallow inter-
val observed in the last two swallows was sometime compensated
by a high volume respiratory cycle beginning with inspiration (see
Fig. 3). Compensatory respirations were usually more frequent in
the 100 ml than the 50 ml SWS. The 100 ml SWS also showed long-
er swallowing apnea periods, greater number of swallows, and
longer duration of swallowing. This kind of compensatory swallow
during the apnea period was reported in previous SWS studies
(Daniels and Foundas, 2001; Dosier et al., 2006; Lederle et al.,
2011). It was also reported that a tendency to inspire during and
after the SWS suggest that there might be an increased drive to
breath during sequential swallowing (Lederle et al., 2011; Dosier
et al., 2006). During the swallowing apnea period, the most impor-
tant swallowing stage is the pharyngeal phase from the standpoint
of respiration control, because swallowing and respiration share
the pharynx as a common pathway during the pharyngeal phase
of swallowing (Thexton et al., 2007). Swallowing itself is also ac-
cepted as a protective reex for the upper airway, while respiration
is also a reliable system to control the rhythmicity and regularity of
SWS. Experimental studies demonstrated that the CPG of breathing
and swallowing may anatomically overlap but the grouping of the
medullary interneurons may have more than one function, or the
two system of respiration and swallowing are coordinated during
SWS (Jean, 2001; Jean and Dallaporta, 2006; Kessler and Jean,
1985; Martin, 2006). It is conceivable that the very rst swallows
should be under voluntary control (Aydogdu et al., 2011) but in
subsequent swallow sequences are inuenced some automated
or reexive process. Later swallows and their interswallow inter-
vals might be regulated by the swallowing CPG in the brainstem
network, and the NTS may be important for this regulation (Jean,
2001; Car and Amri, 1987). An inherent feature of the generator
neurons at the dorsal swallowing group (DSG) in and around the
NTS is to re a sequential or rhythmic pattern parallel to the motor
pattern of oropharyngeal swallowing (Bariotay et al., 2008; Felix
et al., 2006; German et al., 2009; Jean, 2001; Jean and Dallaporta,
2006). The bulbar CPG and the NTS could also functionally impor-
tant in controlling the rhythmicity of SWS in humans; rhythmicity
of SWS is disturbed in patients with amyotrophic lateral sclerosis
(ALS) especially in bulbar and pseudobulbar types (Aydogdu
et al., 2011).
In our 50 and 100 ml SWS, heart rate signicantly increased
during swallowing apnea (p = 0.001). Swallowing tachycardia is
one characteristic of the SWS apnea period. This has been previ-
ously investigated, usually by discrete swallows; drinking water
was shown to cause a transient increase in sympathetic activity,
mean arterial pressure, and heart rate immediately after drinking
 N. Grgr et al. / Journal of Electromyography and Kinesiology 23 (2013) 619626
(Endo et al., 2001; Nitta et al., 2003). It was concluded that the ra-
pid rise in blood pressure and increase in heart rate might be due
to oropharyngeal stimulation, swallowing induced factors, and/or
feed forward mechanisms by a control descending signal from
higher brain centers (Endo et al., 2002, 2001). It was also important
when use the SWS as the test for elderly patients.
4.3. Termination of SWS
When the SWS process is terminated, some neurophysiological
and respiratory changes can be observed. Almost all our normal
participants initiated the swallowing apnea with expiration but
the nish it with either expiration or inspiration at the end of swal-
lowing apnea in SWS; while the inspiration could often encoun-
tered tested with 100 ml SWS in young patients. This also
supports the thought that the 100 ml SWS for young dysphagic pa-
tients would be risky and increase the probability of the escape of
foods or water into the upper airway at the end of swallowing ap-
nea with inspiration. The increased inspiration at the end of swal-
lowing apnea in SWS has been previously reported (Lederle et al.,
2011; Dosier et al., 2006).
Swallowing tachycardia immediately ceased after termination
of swallowing apnea, but we should be aware that patients with
cardiac rhythm disorders should be carefully monitored during
the SWS test.
Finally, a SSR was evoked at termination of the SWS or slightly
later in 30 participants after the 50 ml SWS and in 27 participants
after the 100 ml SWS (Fig. 6). Thus approximately 52% of normal
adults may have SSR at the end of SWS. The occurrence of SSR at
termination of SWS should not be accepted as a kind of arousal.
This SSR at termination of SWS could be either related to the
peripheral effects of oropharyngeal swallowing; especially late ef-
fect of respiratory changes or second SSR should also be originated
from central mechanisms related with brainstem processes but
further studies are required to elucidate these speculations. We
may point out that the second SSR is absent when the arousal
SSR could not appear at the same SWS.
4.4. Aging effects on the SWS
SWS parameters did not signicantly differ between young and
older subjects with the exception of the swallowing apnea period,
which was signicantly prolonged in the older age group on the
50 ml SWS (p < 0.04). This may be the result of our age cut-off, as
a higher cut-off of 70 years may show more differences. From this
point, we may have two obstacle;
(a) the lower limit of upper age should be over 70 years old.
(b) Our healthy participants were not so many to elucidate age
differences.
In spite of these points; we have to be careful using SWS in old
people and patients with neurogenic dysphagia.
The SWS method have been demonstrated to give frequent
swallowing abnormalities in patients with dysphagia determined
either by videouoroscopy (Daniels and Foundas, 2001; Dosier
et al., 2006) or by electrophysiologically methods of SWS (Aydogdu
et al., 2011). The SWS methods described in this study could also
be possible to demonstrate the dysphagia due to airway problems
in attention with chronic obstructive lung disease or obstructive
sleep apnea. In this kind disorders, dysphagia produced by the air-
way problems instead of central nervous disorders.
625
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_
Nevin Grgr was born at 1965 in Izmir. She graduated
from Ege University Medical School in 1989. During
19931996 period, she completed her education at
Neurology Department of Atatrk Research and Train-
_
ing Hospital in Izmir. Then, she worked as Neurologist at
the same hospital. She worked in EMG laboratory of
Clinical Neurophysiology Department of Ege University
Medical School for 6 months in 2000. She has been
working as neurologist at Neurology Department of
_
Atatrk Research and Training Hospital in Izmir since
2000. She is a member and Turkish Society of Clinical
Neurophysiology EEG-EMG. Her research interests focus
on epilepsia and clinical neurophysiology.
S
ehnaz Arc was born at 1973 in Antalya. She gradu-
ated from Akdeniz University Medical School in 1996.
She completed her education at Neurology Department
of Ege University Medical School Hospital in Izmir and
she became Neurologist in 2003. She has been working
as neurologist at Neurology Department of Atatrk
_
Research and Training Hospital in Izmir since 2003. She
is a member of Turkish Society of Neurology and Turk-
ish Society of Clinical Neurophysiology EEGEMG. Her
research interests focus on epilepsia and clinical neu-
rophysiology.
Tlay Kurt Incesu was born at 1967 in Samsun. She
graduated from Gazi University Medical School, Ankara
in 1990. During 19941998 period, she completed her
education at Neurology Department of Pamukkale Uni-
versity Medical School Hospital in Denizli and she
became Neurologist. Then, she worked as assistant
professor at the same hospital. She worked in EMG
laboratory of Clinical Neurophysiology Department of
Ege University Medical School for 6 months in 2000. She
has been working as an associate professor at Neurology
Department of Medical School, Katip Celebi University
_
in Izmir since 2011. She is a member of Turkish Society
of Neurology and Turkish Society of Clinical Neurophysiology EEG-EMG. Her
research interest focus on clinical neurophysiology and movement disorders.
Yaprak Seil was born at 1971 in Sakarya. She gradu-
ated from Istanbul University Cerrahpasa Medical
School (English Department) in 1995. She completed
her education at Neurology Department of Ege Univer-
sity Medical School Hospital in Izmir and she became
Neurologist in 2001. Then, she worked as volunteer
neurologist for one year in EMG laboratory of Clinical
Neurophysiology Department at the same hospital. She
has gained Young Scientist Award from Turkish Acad-
emy of Sciences in January 2002. Also, she and swal-
lowing group of Clinical Neurophysiology Department
of Ege University had Sedat Simavi Medical Sciences
Award in 2003. She has been working at Neurology Department of Atatrk Edu-
_
cation and Research Hospital in Izmir since 2002, after 2007 she has been associate
proffessor at the same department. She is a member of Turkish Society of Neurology
focus on clinical neurophysiology, neurourology-sexual disorders in females and
neuromuscular disorders.
Figen Tokucoglu graduated from Aegen University
Medical School in 1989. She completed her residency on
neurology in 1995, had master degree on elctrodiag-
nostic neurology. Her area of interests are clinical
electrophysiology, movement disorders and multiple
sclerosis.
Cumhur Ertekin is a professor in neurology and clinical
neurophysiology. He was a chair in clinical neurology at
_
Ege University in Izmir, Turkey. He was founder of
Turkish Society of Clinical Neurophysiology EEGEMG.
He was retired from University.