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Dysphagia in Alzheimer's disease

Article in Neurophysiologie Clinique/Clinical Neurophysiology · February 2016

DOI: 10.1016/j.neucli.2015.12.007

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ORIGINAL ARTICLE/ARTICLE ORIGINAL

Dysphagia in Alzheimer’s disease

Dysphagie dans la maladie d’Alzheimer

Yaprak Seçil a,∗, Şehnaz Arıcı a, Tülay Kurt İncesu a,

Nevin Gürgör a, Yeşim Beckmann a, Cumhur Ertekin b

a
Neurology Department, Katip Çelebi University Atatürk Training and Research Hospital, Basın Sitesi,
35360 Izmir, Turkey
b
Department of Clinical Neurophysiology, Ege University Medical School Hospital, Izmir, Turkey

Received 21 January 2015; accepted 29 December 2015

Available online 11 May 2016

KEYWORDS Summary
Alzheimer’s disease; Objective. — To investigate electrophysiological parameters of swallowing in all stages of
Deglutition; Alzheimer’s disease.
Dementia; Methods. — Forty Alzheimer’s disease patients, 20 age-matched normal controls and 20 young
Electrophysiology; normal controls were included. Dysphagia limit (DL) and sequential water swallowing (SWS)
Swallowing tests were performed. Cardiac rhythm, respiration and sympathetic skin responses were con-
comitantly recorded.
Results. — Dysphagia was found in 30/40 (75%) of Alzheimer’s disease patients. Mean volume at
the DL test was significantly reduced (16.5 ± 1.0 mL) in the Alzheimer’s disease group. Swallow-
ing and apnea times in the SWS test were significantly prolonged in elderly controls, but even
longer in Alzheimer’s disease patients.
Conclusions. — Alzheimer’s disease patients had electrophysiological features of dysphagia,
even in the early period of disease. The cortical involvement and severity of cognitive dis-
order can increase swallowing problems, but subclinical signs of dysphagia may be observed
even in patients with mild or moderate Alzheimer’s disease.
© 2016 Elsevier Masson SAS. All rights reserved.

Résumé
MOTS CLÉS Objectif. — Évaluer par des mesures électrophsyiologiques le temps oro-pharyngien de la dég-
Déglutition ; lution dans la maladie d’Alzheimer à différents stades.
Démence ; Méthodes. — Quarante patients atteints de maladie d’Alzheimer, 20 témoins normaux appariés
Électrophysiologie ; en âge, et 20 jeunes sujets sains ont été inclus. Les tests de « limite de dysphagie » et de dég-
Maladie d’Alzheimer lutition séquentielle d’eau ont été réalisés. Le rythme cardiaque, la respiration et les réponses
cutanées sympathiques ont été enregistrées de façon concomitante.
∗ Corresponding author. Tel.: +905325469802.
E-mail address: ysecil@gmail.com (Y. Seçil).

http://dx.doi.org/10.1016/j.neucli.2015.12.007
0987-7053/© 2016 Elsevier Masson SAS. All rights reserved.
172 Y. Seçil et al.

Résultats. — Une dysphagie a été trouvée dans 30/40 [75 %] chez les patients d’Alzheimer. Le
volume moyen au test de « limite de dysphagie » était significativement réduit (16,5 ± 1,0 mL)
chez les patients d’Alzheimer. Dans le test de déglutition séquentielle d’eau, les temps de
déglutition et d’apnée étaient prolongés chez les témoins âgés, et de façon beaucoup plus
significative chez les patients d’Alzheimer.
Conclusions. — Les patients atteints de maladie d’Alzheimer avaient des signes électrophysi-
ologiques de dysphagie, même au début de la maladie. L’implication corticale et la sévérité
des troubles cognitifs peuvent augmenter les troubles de déglutition mais des signes infra-
cliniques de dysphagie peuvent être décelés même chez des patients ayant une forme légère
ou modérée de maladie d’Alzheimer.
© 2016 Elsevier Masson SAS. Tous droits réservés.

Introduction
Dysphagia or swallowing impairment is an important symp-
tom in dementia. It has been estimated that up to 45% of
patients with dementia have some degree of swallowing dif-
ficulties [25,51]. After 65 years, prevalence of dementia
increases, and after 85 years it increases up to 30% [24,42].
Because Alzheimer’s disease [AD] dementia is generally a
disease of the elderly population, there are some overlaps
between normal elderly and dementia groups. The subtle
physiological changes in the elderly and early period of AD
should be differentiated, at least regarding the peripheral
aspects of oropharyngeal swallowing. Dysphagia is gener-
ally expected in moderate and late stages of AD [12,25,48].
However, it can be observed in the early period as subclinical
dysphagia, which may be shown by using some swallowing
test methods [26,28,44,54]. In mild to moderate AD, inap-
propriate eating, indifference to food and eating, choking
and aspiration symptoms may occur [48]; feeding and swal-
lowing apraxia may also be observed in AD patients [48].
Various cortical areas control oropharyngeal swallowing
[23,39,50,55] and these may be affected by AD pathol-
ogy, including the insula, frontal anterior cingulate cortex,
primary motor and sensory motor cortical areas and sup-
plementary motor areas [8,26,27,39]. As a result, it is
commonly believed that involvement of swallowing corti-
cal areas by the cortical pathological process of AD is the
main cause of dysphagia observed in this condition.
Oropharyngeal dysphagia in AD is an important issue
because aspiration during swallowing can cause aspira-
tion pneumonia during the course of the disease. Even
in the early stage of AD, patients can suffer pneumonia
due to ‘‘silent’’ aspiration occurring in these patients [31].
The early clinical problem in AD patients with oropharyn-
geal dysphagia is subtle, such that patients may not be
aware of swallowing difficulties resulting in silent aspira-
tion. Videofluoroscopy [VFS] and fiberoptic endoscopy [FEES]
are methods that can clearly demonstrate the aspiration
[1,36] and are suitable for use in AD patients [32]. However,
VFS and FEES need special equipments and skilled techni-
cal personnel; in addition, they may not be easy to apply
in some AD patients because of communication and cog-
nition problems [6,13]. Non-invasive and easily applicable
electrophysiological swallowing tests have been developed
[5,14,15,22]. Mild to moderate and even sometimes severe
cognitive impairment should not be an obstacle for electro-
physiological assessment. The neurophysiological test called
the ‘‘dysphagia limit’’ has been used and found useful in frail
elderly patients even with severe cognitive decline. Despite
older age and cognitive decline, all participating patients
were easily fed orally [3,7].
Our aim in this study is to investigate oropharyngeal swal-
lowing in mild, moderate and severe stages of AD patients
and compare these with age-matched elderly and young
healthy participants, using electrophysiological methods.
We hypothesized that AD patients may be dysphagic even in
the early period of disease and that this would be not merely
be due to the aging process. Although swallowing problems
and dysphagia form a continuum, there are two main clini-
cal presentations of dysphagia. The first occurs in the early
period of AD when the patients are still able to collaborate
in most diagnostic tests, such as swallowing EMG tests. The
second type of dysphagia occurs in the later stages of AD, in
patients who have severe cognitive impairment and in whom
the dysphagia has an apraxic pattern.
Methods
Forty AD patients [55—86 years] diagnosed according to
NINCDS-ADRDA 1984 criteria [also revised in 2011] who
were able to participate in electrophysiological investiga-
tion were enrolled in this study from the AD outpatient
clinic of our hospital. Twenty age-matched normal controls
[AMNCs] [63—87 years] and 20 young normal controls [YNCs]
[23—39 years] without any known systemic disease such as
diabetes mellitus, any known malignancy or rheumatological
diseases were included in the study. The AD patients were
29 women [75.34 ± 6.88 years] and 11 men [72.54 ± 8.41
years]; the mean age was 74.57 ± 7.33 years. The AMNCs
were 15 women [72.4 ± 7.11] and 5 men [76.6 ± 7.09], with
mean age of 73.45 ± 7.17 years. The YNCs were 9 women
[29.6 ± 4.87] and 11 men [32.45 ± 3.93], with mean age of
31.2 ± 4.49 years.
Patients were classified in the outpatient clinic as having
mild [n = 11, 61—81 years, MMSE between 20—28], moder-
ate [n = 20, 57—86 years, MMSE between 12—19] or severe
dementia [n = 9, 55—85 years, Mini Mental State Examination
[MMSE] between 3—10] by using the Clinical Dementia Rat-
ing scale [CDR]. CDR 0.5—1 is accepted to be mild, CDR 2
is moderate and CDR 3 is severe. Only patients who were
able to perform the test were included in the study. In
the severe group, MMSE results were very low but patients
were cooperative and they could perform the test. Before
Dysphagia in AD
Figure 1 Dysphagia limit (DL) test in an age-matched normal control (A) and a patient with Alzheimer’s disease (B). DL was 10 mL.
Each swallow is indicated by an arrow in the upper traces corresponding to submental/suprahyoid electromyography (SM-EMG). The
second traces correspond to respiratory signals.
electrophysiological assessment, all patients and normal
controls were examined neurologically and physically. Swal-
lowing difficulties were asked about and noted. In clinical
assessment, no swallowing difficulty was reported, except
by one AD patient who had moderate dementia. All patients
were taking acetylcholine esterase inhibitors, memantine
or combination therapy according to disease severity. MMSE
was performed in all patients [mean 15.53 ± 5.85]; in
the mild AD group this was 22.63 ± 2.73, in moderate
14.85 ± 2.39 and in severe groups 7.5 ± 2.32.
Demographic data were recorded. The ethics committee
of our hospital approved this study and informed consent
was obtained from patients and controls.
Each subject was instructed to sit on a chair and hold his
or her head in a neutral upright position. Swallowing signals
were recorded from submental/suprahyoid electromyog-
raphy [SM-EMG] recorded using bilateral silver [Ag] cup
electrodes taped under the chin over the submental muscle
complex in the first channel. In the second channel, respira-
tory signals were obtained via a nasal cannula [Sleep Sense® ]
and placed at the entry of the nostrils and connected to
the EMG machine. Inspiration and expiration respiratory
movements were recorded synchronously. In the third chan-
nel, we simultaneously recorded electrocardiogram [ECG]
data using silver cup electrodes one of them placed on
the second left intercostal space and second placed on the
dorsum of the left hand. In the fourth channel, the sym-
pathetic skin response (SSR) was recorded from the skin of
the left hand; Ag electrodes were placed on the skin of the
173
palm and dorsum of the hand using electrogel [Lome EEG
paste].
At the beginning of the electrophysiological test, basal
heart rate and respiration frequency were examined and
recorded at rest; patients were instructed not to move
and swallow during this recording. Basal heart and respira-
tion rates were calculated. After basal recording, dysphagia
limit [DL] [3,14—16] and 50 mL sequential water swallowing
[SWS] tests were studied in all groups [2,4,22]. In severe
group, some of the swallowing tests were performed with
difficulty, but the evaluation was completed because all
severely affected patients, even those with MMSE as low
as 3, performed swallowing automatically when they were
given a water cup. They had no motor disability. Some severe
patients with orobuccal apraxia were included and are dis-
cussed below.
Dysphagia limit [DL]
Consecutively increasing 5,10,15 and 20 mL volumes of
water were given to patients by a graduated syringe, and
they were asked to keep the water in their mouth. They
were instructed to swallow by examiners; the ‘‘swallow’’
command for DL examination showed us the maximal liq-
uid swallowing capacity of patient. Normal DL is more than
20 mL in normal subjects (Fig. 1). If a person can swallow
20 mL normally, DL is normal. Patients or normal controls
with DL of 20 mL or less were considered to be dysphagic
174
Figure 2 A 50 mL sequential water swallowing (SWS) test in
an age-matched normal control (A) and a patient with severe
Alzheimer’s disease (B). Foreburst can be seen at the begin-
ning of the upper traces corresponding to submental/suprahyoid
electromyography. Swallows are indicated by arrows, as well
as swallowing duration. The second traces correspond to
respiratory signals, including the duration of swallowing-
associated apnea duration. The third traces correspond to
electrocardiographic signals. The fourth traces correspond to
swallowing-induced sympathetic skin reflex (SSR). In patient’s
recordings (B), swallowing and swallowing-associated apnea
durations are longer than normal and no SSR was recorded. Total
analysis time: 20 seconds.
(Fig. 1) [15,16]. SSRs during DL were evaluated; these were
considered to be absent if SSR was not recorded during any
amount of water swallowing including 50 mL SWS.
Sequential water swallowing [SWS]
Sequential water swallowing (SWS) is a test demonstrating
maximal duration of SM-EMG and apnea periods during con-
tinuous drinking of 50 mL water. During SWS, patients were
instructed to drink 50 mL tap water from a standard dispos-
able plastic cup in a normal fashion. The number of swallows
was counted from the periodic movement deflexions of SM-
EMG during SWS. The total duration of SWS was calculated
from the onset of the first to the end of the last swallow
burst on the SM-EMG traces in a SWS epoch (Fig. 2) Dur-
ing SWS respiration, ECG and related sympathetic functions
were also connected to the other channels of EMG apparatus
[22]. Airflow direction was recorded as a negative polarity
representative of inspiration and a positive polarity rep-
resentative of expiration. The SM-EMG and all changes in
respiration were simultaneously recorded to detect swal-
lowing apnea and swallowing period during 50 mL of SWS.
Y. Seçil et al.
The SM-EMG and phase of respiration were simultaneously
recorded to detect beginning of ‘‘swallowing apnea’’, all
calculations were shown in Fig. 2 [22]. Compensatory respi-
ratory cycles [CRC], meaning unexpected respiration during
swallowing apnea period, were recorded. Two or more CRCs
were considered pathological. SSR and heart rate changes
during SWS were also evaluated and reviewed in detail. Dur-
ing 50 mL SWS, the latency difference from the beginning of
the trace to first SM-EMG activity is called SWS latency and
latency difference in all groups was evaluated statistically.
A Nicolet Viking V11.0 EMG machine with four channels was
used for the study.
The mean ± SD and SEM of all measured quantities were
calculated. Group analysis was performed using Mann-
Whitney U and Wilcoxon rank tests. Pearson correlation
tests were used to compare evaluated data. The level of
significance was set at P < 0.05. Statistical analyses were
performed using SPSS 15.0.
Results
DL
Dysphagia was found in 30 out of 40 of AD patients [75%] and
mean DL was 16.5 ± 1.01 mL in AD group. DL was > 20 mL and
normal in both control groups [P < 0.05] (Fig. 1). Dysphagic
patients accounted for 45.5% of mild, 85% of moderate and
89% of the severe AD group. This proportion thus increased
with disease severity. Orobuccal apraxia was observed in
some severe group patients; this could also affect low DL in
the group. During DL examination coughing suggesting laryn-
geal penetration was found in 2/11 of the mild AD group
[18.1%] and 5/20 in moderate group [25%]; no cough was
found in severe group.
Sequential water swallowing
Foreburst of SWS
The foreburst is a first deflexion of SWS; this does not con-
tain water and its incidence was about 90% in normal adults
(Fig. 2) [22]. Absence of foreburst was noted in the AD group.
In our study, foreburst was present in only 40% of all AD
patients while it was present in 90% of the AMNC group
and 85% of the YNC group. There were differences between
stages of AD, since the foreburst was present in 55% of the
mild group, 35% of the moderate and 33% of the late stage
AD group.
Number of swallows
The number of swallows in AD group was increased and
this was statistically significant when compared to YNCs
and AMNCs [P = 0.001, P = 0.009]. When YNCs and AMNCs
were compared there was no difference between groups
[P > 0.05]. This meant that number of swallows did not
change in association with aging. When subgroups of AD were
compared to normals, both AMNCs and YNCs, only the mod-
erate AD group showed statistically significant difference
(Table 1, Fig. 3).
Dysphagia in AD 175

Table 1 Sequential water swallowing test results.

Groups Number of swallows Duration of swallowing Duration of apnea

Mean ± SD Mean ± SD Mean ± SD

s s

AD total 5.65 ± 1.61 (3—10) 9.70 ± 2.73 (4—18) 9.85 ± 2.56 (6—16)
Mild 4.90 ± 0.94 (3—6) 7.36 ± 1.38 (4—9) 7.63 ± 0.80 (6—9)
Moderate 6.05 ± 1.70 (4—10) 9.70 ± 1.98 (6.5—15) 9.80 ± 1.83 (7—14)
Severe 5.66 ± 1.87 (4—9) 12.55 ± 1.87 (7.5—18) 12.66 ± 2.73 (8—16)
AMNCs 4.55 ± 1.09 6.22 ± 1.05 6.30 ± 1.38
YNCs 4.35 ± 0.24 5.50 ± 1.12 5.57 ± 1.57
AD: Alzheimer’s disease; AMNCs: age-matched normal controls; YNCs: young normal controls; SD: standard deviation.

Figure 3 Mean values of swallowing-associated apnea dura-

tion (sec), swallowing time duration (sec), and number of
swallows during a 50 mL sequential water swallowing test.
AMNC: age-matched normal control group; AD: Alzheimer’s dis-
ease groups, according to disease severity.
SWS duration
Date on duration of SWS data is shown in Table 1. SWS dura-
tion was significantly longer in the AD patient group when
compared with both normal control groups [P = 0.000]. It was
also significantly different between control groups, indicat-
ing that aging affects swallowing duration [P = 0.046]. AD
patients have prolonged SWS duration that is even longer
than normal elderly subjects. Also, when we compared
subgroups, all subgroups were statistically different from
both age-matched and young normal controls [P < 0.05] and
swallowing duration increased according to disease severity
(Fig. 3).
Figure 4 Percentage of sympathetic skin responses (SSR) trig-
gered by swallowing during dysphagia limit and sequential water
swallowing tests. AMNC: age-matched normal control group;
YNC: young normal control group; AD: Alzheimer’s disease
groups, according to disease severity.
SSR during SWS and DL
Swallowing-triggered SSR were elicited in 55% of all AD
patients (Fig. 4). SSR was inversely proportional to the sever-
ity of dementia and was significantly different between
AD group and normal controls even in the elderly group
[P < 0.05] (Fig. 4). It was rarely recorded in severe AD group
[34%] while its occurrence was 95% in both control groups.
Although aging is a factor for altered SSR, this was different
between AD group and AMNCs.

Swallowing apnea period

The swallowing apnea period prolongation was significantly
different between AD and NC groups [P = 0.000] (Table 1). In
all AD subgroups [mild, moderate, severe], the apnea period
was significantly longer than normals [P < 0.05] (Fig. 3). The
most prolonged duration was in the AD group while the
AMNC group was still prolonged but not as much as subjects
with AD. Young patients had significantly shorter duration
when compared with AD group [P < 0.05]. However, there Figure 5 Swallowing latency (sec) during a 50 mL sequential
was no significant difference between AMNCs and YNCs. The water swallowing (SWS) test. AD: Alzheimer’s disease group;
severe group had the most prolonged duration in all sub- AMNC: age-matched normal control group; YNC: young normal
groups (Fig. 3, Table 1). CRCs were found in 15% of the AD control group. Latency was significantly longer in the AD group
group, while the proportion was 5% in YNCs and 0% in AMNCs (mean: 2.69 s) compared to the AMNC group (mean: 2.08 s;
[P > 0.05]. P = 0.01) and the YNC group (mean: 1.69; P < 0.001).
176
Figure 6 Apraxic swallowing pattern during a 50 mL sequential water swallowing test in a patient with severe Alzheimer’s disease
(A) and an age-matched normal control (B). The first arrow indicates ‘‘swallow command’’ and the second arrow indicated the
onset of the first swallow. In the AD patient, swallowing latency is clearly delayed (9 seconds) and swallows are not regular. Total
analysis time: 20 seconds.
Swallowing latency during SWS
This parameter was found to be significantly different
between groups. It was longer in the AD group when com-
pared to AMNCs [P = 0.000] and YNCs [P = 0.01] (Fig. 5).
Also, during 50 mL SWS, an apraxic swallowing pattern was
observed, especially in the severe AD group (Fig. 6).
Discussion
Abnormal swallowing is an important concern in AD. Accord-
ing to our study, AD patients have deglutition problems even
in the early period of the disease. We can summarize our
findings in AD as follows:
• about 75% of AD patients were found to be dysphagic in
spite of reporting no swallowing complaints. On the other
hand, AMNCs showed no deglutition problems by using our
electrophysiological methods;
• swallowing problems were clearly progressive. These
started from ‘‘subclinical dysphagia’’, evolving to ‘‘overt
dysphagia’’ and finally ‘‘swallowing apraxia’’ as a contin-
uum.
There are probably different kinds of pathology related
to swallowing disorders: one is classical dysfunction of
swallowing, as may be observed in all other degenerative
disorders with dysphagia such as Parkinson’s disease [19,43],
ALS [5,17,13], progressive suprabulbar syndrome of vascu-
lar origin and Wallenberg syndrome [4,18]. However in AD,
another pathological process is added to the clinical picture:
severe cognitive dysfunction was associated with swallowing
apraxia (e.g. the patient remembering how to swallow the
bolus), the so-called dyspraxia of swallowing [12,21,32,37].
Dysphagia may be a consequence of normal aging; there-
fore, the dysphagia observed in our study might theoretically
be related to normal aging in AD patients. The prevalence of
swallowing disorders or dysphagia in older individuals ranges
from 7 to 30% [12,51]. Dysphagia affects up to 68% of elderly
nursing home residents [47,51], 30% of elderly admitted to
hospital [33] and 13—38% of elderly who live independently
[29,45,46]. However, it is obvious that our patients with
AD were not solely affected due to aging since all elec-
trophysiological swallowing parameters were normal in our
age-matched normal older group.
Y. Seçil et al.
It is estimated that the prevalence of dysphagia in
AD is nearly 45% as judged on a clinical basis [25]. As
previously mentioned, our DL and SWS data in AD were
significantly abnormal when compared to AMNC [P < 0.05]
[25]. Such prevalence estimations have generally been
based on clinical examinations and patient questionnaires.
Our electrophysiological method is objective and has the
advantage of detecting subclinical dysphagia in up to
75% of cases. Although videofluoroscopic studies are inva-
sive and may be difficult to utilise in dementia patients,
they were found to be effective in detecting abnormal
swallowing function including aspiration in high percent-
ages [25,38]. However because it remains difficult to use
such methods in patients with AD, non-invasive meth-
ods for swallowing assessment such as water swallowing
tests are preferred [10,20,30,41,49]. Electrophysiological
methods have indeed been found useful to detect sub-
clinical dysphagia in various severe neurological disorders
[4,13,17—19,22].
In patients with AD, swallowing problems are progres-
sive from ‘‘subclinical dysphagia’’ to ‘‘overt dysphagia’’ and
then ‘‘swallowing apraxia’’. Incidence of swallowing abnor-
mality in AD was increased from 45.5% in the mild group
to 89% in the severe group by using the DL test. Since the
DL test indicates the dysphagia objectively and numerically
[3], stepwise increase in DL abnormality according to dis-
ease severity shows that swallowing abnormality follows a
progressive pattern in AD patients. There may be a subclini-
cal period before the onset of clinically overt dysphagia in
AD patients.
Further evidence for the chronic progressive course of
swallowing dysfunction of AD comes from the SWS tests
(Fig. 3). The mean duration of SWS in SM muscle and the
apnea period were significantly and progressively increased
in patients with AD according to classification as mild-
moderate or severe cases. In advanced patients, a severely
prolonged apnea period, probably because of pseudorhyth-
micity of SWS, appeared to be related to decreased cognitive
status and related swallowing apraxia. This swallowing pat-
tern resulted in random swallows during SWS. In conclusion,
on the basis of electrophysiological findings, swallowing
problems start early in the disease course even before clin-
ical signs and symptoms become objective. Similar reports
are compatible with our conclusion that dysphagia is seen
not only in late stages but also in the early stages of the AD
[26,54].
Dysphagia in AD
Finally, our data suggest that there may be different
mechanisms for swallowing disorders in AD. The first is clas-
sical dysfunction of swallowing such as may occur in all
other degenerative cortico-subcortical diseases that have
dysphagia symptoms for example Parkinson’s disease, which
is main movement disorder causing dysphagia with non-
dopaminergic mechanisms [40,52]. Besides this classical
data, our electrophysiological evidence showed that the
latency of swallowing onset in AD was significantly delayed
and that this was much more abnormal in severe AD cases
than in milder ones (Figs. 4 and 5). Some studies have pro-
posed that delayed SWS could be result of sensory deficit
in the oral cavity [1,48]. However, such intraoral sensory
deficit could rather be the cause of early bolus escape into
the pharynx and may cause aspiration before the beginning
of swallowing [34,35]. Furthermore, we did not find cough as
an important indicative sign for laryngeal penetration in our
cases, either in mild or moderate AD cases. Additionally the
age of severe AD patients did not significantly differ from the
other groups. Delayed pharyngeal response and prolonged
oral phase were mostly seen in severe cases. Results were
correlated with disease severity [P < 0.05]. If we look again
at Fig. 6, after the examiner’s swallow command the onset
of first swallow was tremendously delayed when compared
with a normal control. This electrophysiological finding can-
not be explained either by reduced intraoral sensitivity or
other peripheral oropharyngeal disturbances. In these cases,
auditory pathways seemed to be normal because patients
were able to obey all commands in this aspect. Swallowing
reaction time was found to be delayed due to central factors
especially reduced cognition.
The swallowing-triggered SSR was an indicator for
a central delay mechanism in AD patients (Fig. 4).
While swallowing-triggered SSR percentage progressively
decreased according to disease severity, absence of SSR per-
centage was significantly increased in the whole AD group.
This finding was compatible with cortical disturbance. Per-
sistence of SSR was related to arousal and functionality
of cortex and ascending reticular activating system. If we
exclude peripheral factors, this kind of SSR arousal most
likely reflects altered attentional, emotional and arousal
conditions expected during such a task [9,53].
It might be proposed that an arousal/attentional
response is important for the safety of the swallow. Such
autonomic and visceromotor activities may be localized in
the anterior cingulate cortex [11,39]. Manipulation of atten-
tion and concentration could also be shown to evoke SSR just
by inspiration of SWS [2]. The delay of SWS is thus related to
cognitive function in AD, and we agree with other authors
that this kind of swallowing problem should be termed swal-
lowing apraxia [1,26,32,37].
Disclosure of interest
The authors declare that they have no competing interest.
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