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