Introduction: People with diabetes frequently have gastrointestinal problems and related deglutition disorders. Objective: The aims of the present study are to determine the symptomatic swallowing complaints and to evaluate the functionality of oropharyngeal swallowing in patients with type 2 diabetes mellitus (T2DM) by using the Turkish Eating Assessment Tool-10 (T-EAT-10) and fiberoptic endoscopic evaluation of swallowing (FEES). Methods: In this descriptive cross-sectional study, the T-EAT-10 questionnaire was completed by 121 patients with diabetes, and FEES was planned for each individual whose baseline score of the T-EAT-10 was ≥3. Before swallowing trials via samples of nectar-thick consistency, laryngeal sensation and severity of secretion in the hypopharynx were observed. While the swallowing safety was determined using the Penetration-Aspiration Scale (PAS), the Yale Pharyngeal Residue Severity Rating Scale was used to assess the swallowing efficiency. Results: Of the total participants, 22.3% (n = 27) were found to have abnormal swallowing function (T-EAT-10 ≥3), 27.3% (n = 33) had concomitant neuropathy and 28.1% (n = 34) mentioned a reflux complaint. The results of the multivariate linear regression analysis exposed that the T-EAT-10 score was significantly associated with neuropathy (r = 3.763, p < 0.001) and reflux complaint (r = 2.254, p = 0.031). Of the total FEES-tested subjects (n = 20), 95% (n = 19) had a safe swallowing function (PAS = 1). However, diminished laryngeal sensation, increased secretion and presence of residue revealed that patients with T2DM who have self-reported swallowing difficulties have reduced swallowing efficiency. Conclusions: This study has demonstrated that almost 1 out of 4 T2DM patients reported to have swallowing-related problems, and the score of the T-EAT-10 was found to be independently associated with both neuropathy and reflux complaint. FEES results pointed out that swallowing efficiency was relatively reduced in the target population. However, further research is still necessary before obtaining a definitive answer to oropharyngeal swallowing problems in patients with T2DM.

1.
Adeghate
E
,
Schattner
P
,
Dunn
E
.
An update on the etiology and epidemiology of diabetes mellitus
.
Ann N Y Acad Sci
.
2006
Nov
;
1084
(
1
):
1
29
.
[PubMed]
0077-8923
2.
Shaw
JE
,
Sicree
RA
,
Zimmet
PZ
.
Global estimates of the prevalence of diabetes for 2010 and 2030
.
Diabetes Res Clin Pract
.
2010
Jan
;
87
(
1
):
4
14
.
[PubMed]
0168-8227
3.
Baynes
H
.
Classification, pathophysiology, diagnosis and management of diabetes mellitus
.
J Diabetes Metab
.
2015
;
6
(
5
):
1
9
.2155-6156
4.
Association
AD
.
Diagnosis and classification of diabetes mellitus
.
Diabetes Care
.
2014
;
37
(
1
Supplement_1
):
81
90
.
[PubMed]
0149-5992
5.
Hüppe
D
,
Tegenthoff
M
,
Faig
J
,
Brunke
F
,
Depka
S
,
Stuhldreier
M
, et al.
Esophageal dysfunction in diabetes mellitus: is there a relation to clinical manifestation of neuropathy?
Clin Investig
.
1992
Sep
;
70
(
9
):
740
7
.
[PubMed]
0941-0198
6.
Feldman
EL
,
Nave
KA
,
Jensen
TS
,
Bennett
DL
.
New horizons in diabetic neuropathy: mechanisms, bioenergetics, and pain
.
Neuron
.
2017
Mar
;
93
(
6
):
1296
313
.
[PubMed]
0896-6273
7.
Matsuo
K
,
Palmer
JB
.
Anatomy and physiology of feeding and swallowing: normal and abnormal
.
Phys Med Rehabil Clin N Am
.
2008
Nov
;
19
(
4
):
691
707
.
[PubMed]
1047-9651
8.
Feldman
M
,
Schiller
LR
.
Disorders of gastrointestinal motility associated with diabetes mellitus
.
Ann Intern Med
.
1983
Mar
;
98
(
3
):
378
84
.
[PubMed]
0003-4819
9.
Bytzer
P
,
Talley
NJ
,
Leemon
M
,
Young
LJ
,
Jones
MP
,
Horowitz
M
.
Prevalence of gastrointestinal symptoms associated with diabetes mellitus: a population-based survey of 15,000 adults
.
Arch Intern Med
.
2001
Sep
;
161
(
16
):
1989
96
.
[PubMed]
0003-9926
10.
Zakaria
DA
,
Bekhet
MM
,
Khodeir
MS
,
Bassiouny
SS
,
Saleh
MM
.
Oropharyngeal Dysphagia and Diabetes Mellitus: Screening of 200 Type 1 and Type 2 Patients in Cairo, Egypt
.
Folia Phoniatr Logop
.
2018
;
70
(
3-4
):
134
7
.
[PubMed]
1021-7762
11.
Gatopoulou
A
,
Papanas
N
,
Maltezos
E
.
Diabetic gastrointestinal autonomic neuropathy: current status and new achievements for everyday clinical practice
.
Eur J Intern Med
.
2012
Sep
;
23
(
6
):
499
505
.
[PubMed]
0953-6205
12.
Frokjaer
JB
,
Andersen
SD
,
Ejskjaer
N
,
Funch-Jensen
P
,
Drewes
AM
,
Gregersen
H
.
Impaired contractility and remodeling of the upper gastrointestinal tract in diabetes mellitus type-1
.
World J Gastroenterol
.
2007
Sep
;
13
(
36
):
4881
90
.
[PubMed]
1007-9327
13.
Borgström
PS
,
Olsson
R
,
Sundkvist
G
,
Ekberg
O
.
Pharyngeal and oesophageal function in patients with diabetes mellitus and swallowing complaints
.
Br J Radiol
.
1988
Sep
;
61
(
729
):
817
21
.
[PubMed]
0007-1285
14.
Restivo
DA
,
Marchese-Ragona
R
,
Lauria
G
,
Squatrito
S
,
Gullo
D
,
Vigneri
R
.
Botulinum toxin treatment for oropharyngeal dysphagia associated with diabetic neuropathy
.
Diabetes Care
.
2006
Dec
;
29
(
12
):
2650
3
.
[PubMed]
0149-5992
15.
Fattori
B
,
Siciliano
G
,
Santoro
A
,
Romeo
SO
,
Nacci
A
.
Fiberoptic Endoscopic Evaluation of Swallowing as possible index of ALS clinical development.
2016
;2(2):27-30.
16.
Hamdan
AL
,
Jabbour
J
,
Nassar
J
,
Dahouk
I
,
Azar
ST
.
Vocal characteristics in patients with type 2 diabetes mellitus
.
Eur Arch Otorhinolaryngol
.
2012
May
;
269
(
5
):
1489
95
.
[PubMed]
0937-4477
17.
Demir
N
,
Serel Arslan
S
,
İnal
Ö
,
Karaduman
AA
.
Reliability and Validity of the Turkish Eating Assessment Tool (T-EAT-10)
.
Dysphagia
.
2016
Oct
;
31
(
5
):
644
9
.
[PubMed]
0179-051X
18.
Belafsky
PC
,
Mouadeb
DA
,
Rees
CJ
,
Pryor
JC
,
Postma
GN
,
Allen
J
, et al.
Validity and reliability of the Eating Assessment Tool (EAT-10)
.
Ann Otol Rhinol Laryngol
.
2008
Dec
;
117
(
12
):
919
24
.
[PubMed]
0003-4894
19.
Langmore
SE
. Endoscopic evaluation of oral and pharyngeal phases of swallowing. GI Motility online. [cited 2019 Sep 15]. Available from: https://www.nature.com/gimo/contents/pt1/full/gimo28.html?ref=binfind.com/web
20.
Langmore
SE
,
Aviv
JE
.
Endoscopic procedures to evaluate oropharyngeal swallowing. Endoscopic evaluation and treatment of swallowing disorders New York
.
Thieme
;
2001
. pp.
73
100
.
21.
Leow
LP
,
Beckert
L
,
Anderson
T
,
Huckabee
ML
.
Changes in chemosensitivity and mechanosensitivity in aging and Parkinson’s disease
.
Dysphagia
.
2012
Mar
;
27
(
1
):
106
14
.
[PubMed]
0179-051X
22.
Murray
J
,
Langmore
SE
,
Ginsberg
S
,
Dostie
A
.
The significance of accumulated oropharyngeal secretions and swallowing frequency in predicting aspiration
.
Dysphagia
.
1996
;
11
(
2
):
99
103
.
[PubMed]
0179-051X
23.
Neubauer
PD
,
Rademaker
AW
,
Leder
SB
.
The Yale Pharyngeal Residue Severity Rating Scale: An Anatomically Defined and Image-Based Tool
.
Dysphagia
.
2015
Oct
;
30
(
5
):
521
8
.
[PubMed]
0179-051X
24.
Colodny
N
.
Interjudge and intrajudge reliabilities in fiberoptic endoscopic evaluation of swallowing (fees) using the penetration-aspiration scale: a replication study
.
Dysphagia
.
2002
;
17
(
4
):
308
15
.
[PubMed]
0179-051X
25.
Koo
TK
,
Li
MY
.
A guideline of selecting and reporting intraclass correlation coefficients for reliability research
.
J Chiropr Med
.
2016
Jun
;
15
(
2
):
155
63
.
[PubMed]
1556-3707
26.
Folwaczny
C
,
Riepl
R
,
Tschöp
M
,
Landgraf
R
.
Gastrointestinal involvement in patients with diabetes mellitus: part I (first of two parts). Epidemiology, pathophysiology, clinical findings
.
Z Gastroenterol
.
1999
Sep
;
37
(
9
):
803
15
.
[PubMed]
0044-2771
27.
Zhao
J
,
Frøkjaer
JB
,
Drewes
AM
,
Ejskjaer
N
.
Upper gastrointestinal sensory-motor dysfunction in diabetes mellitus
.
World J Gastroenterol
.
2006
May
;
12
(
18
):
2846
57
.
[PubMed]
1007-9327
28.
Hamdan
AL
,
Kurban
Z
,
Azar
ST
.
Prevalence of phonatory symptoms in patients with type 2 diabetes mellitus
.
Acta Diabetol
.
2013
Oct
;
50
(
5
):
731
6
.
[PubMed]
0940-5429
29.
Tawfik
EA
,
Walker
FO
,
Cartwright
MS
,
El-Hilaly
RA
.
Diagnostic ultrasound of the vagus nerve in patients with diabetes
.
J Neuroimaging
.
2017
Nov
;
27
(
6
):
589
93
.
[PubMed]
1051-2284
30.
Van Acker
K
,
Bouhassira
D
,
De Bacquer
D
,
Weiss
S
,
Matthys
K
,
Raemen
H
, et al.
Prevalence and impact on quality of life of peripheral neuropathy with or without neuropathic pain in type 1 and type 2 diabetic patients attending hospital outpatients clinics
.
Diabetes Metab
.
2009
Jun
;
35
(
3
):
206
13
.
[PubMed]
1262-3636
31.
Ahmed
W
,
Vohra
EA
.
Esophageal motility disorders in diabetics
.
J Pak Med Assoc
.
2004
Dec
;
54
(
12
):
597
601
.
[PubMed]
0030-9982
32.
Faraj
J
,
Melander
O
,
Sundkvist
G
,
Olsson
R
,
Thorsson
O
,
Ekberg
O
, et al.
Oesophageal dysmotility, delayed gastric emptying and gastrointestinal symptoms in patients with diabetes mellitus
.
Diabet Med
.
2007
Nov
;
24
(
11
):
1235
9
.
[PubMed]
0742-3071
33.
Jorge
JX
,
Panão
EA
,
Simões
MA
,
Borges
CI
,
Delgado
FJ
,
Coelho
ÁC
, et al.
Esophageal body motility in people with diabetes: comparison with non-diabetic healthy individuals
.
Diabetes Res Clin Pract
.
2012
Jul
;
97
(
1
):
77
81
.
[PubMed]
0168-8227
34.
Roman
S
,
Marjoux
S
,
Thivolet
C
,
Mion
F
.
Oesophageal function assessed by high-resolution manometry in patients with diabetes and inadequate glycaemic control
.
Diabet Med
.
2014
Nov
;
31
(
11
):
1452
9
.
[PubMed]
0742-3071
35.
George
NS
,
Rangan
V
,
Geng
Z
,
Khan
F
,
Kichler
A
,
Gabbard
S
, et al.
Distribution of esophageal motor disorders in diabetic patients with dysphagia
.
J Clin Gastroenterol
.
2017
Nov/Dec
;
51
(
10
):
890
5
.
[PubMed]
0192-0790
36.
Aviv
JE
,
Spitzer
J
,
Cohen
M
,
Ma
G
,
Belafsky
P
,
Close
LG
.
Laryngeal adductor reflex and pharyngeal squeeze as predictors of laryngeal penetration and aspiration
.
Laryngoscope
.
2002
Feb
;
112
(
2
):
338
41
.
[PubMed]
0023-852X
37.
Onofri
SM
,
Cola
PC
,
Berti
LC
,
da Silva
RG
,
Dantas
RO
.
Correlation between laryngeal sensitivity and penetration/aspiration after stroke
.
Dysphagia
.
2014
Apr
;
29
(
2
):
256
61
.
[PubMed]
0179-051X
38.
Kaneoka
A
,
Pisegna
JM
,
Inokuchi
H
,
Ueha
R
,
Goto
T
,
Nito
T
, et al.
Relationship between laryngeal sensory deficits, aspiration, and pneumonia in patients with dysphagia
.
Dysphagia
.
2018
Apr
;
33
(
2
):
192
9
.
[PubMed]
0179-051X
39.
Shapira-Galitz
Y
,
Shoffel-Havakuk
H
,
Halperin
D
,
Lahav
Y
.
Association Between Laryngeal Sensation, Pre-swallow Secretions and Pharyngeal Residue on Fiberoptic Endoscopic Examination of Swallowing
.
Dysphagia
.
2019
Aug
;
34
(
4
):
548
55
.
[PubMed]
0179-051X
40.
Barrett
AM
,
Lucero
MA
,
Le
T
,
Robinson
RL
,
Dworkin
RH
,
Chappell
AS
.
Epidemiology, public health burden, and treatment of diabetic peripheral neuropathic pain: a review
.
Pain Med
.
2007
Sep
;
8
(
2
Suppl 2
):
S50
62
.
[PubMed]
1526-2375
41.
Vinik
AI
,
Nevoret
ML
,
Casellini
C
,
Parson
H
.
Diabetic neuropathy
.
Endocrinol Metab Clin North Am
.
2013
Dec
;
42
(
4
):
747
87
.
[PubMed]
0889-8529
42.
Franklin
GM
,
Kahn
LB
,
Baxter
J
,
Marshall
JA
,
Hamman
RF
.
Sensory neuropathy in non-insulin-dependent diabetes mellitus. The San Luis Valley Diabetes Study
.
Am J Epidemiol
.
1990
Apr
;
131
(
4
):
633
43
.
[PubMed]
0002-9262
43.
Dyck
PJ
,
Kratz
KM
,
Karnes
JL
,
Litchy
WJ
,
Klein
R
,
Pach
JM
, et al.
The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study
.
Neurology
.
1993
Apr
;
43
(
4
):
817
24
.
[PubMed]
0028-3878
44.
Pop-Busui
R
,
Boulton
AJ
,
Feldman
EL
,
Bril
V
,
Freeman
R
,
Malik
RA
, et al.
Diabetic neuropathy: a position statement by the American Diabetes Association
.
Diabetes Care
.
2017
Jan
;
40
(
1
):
136
54
.
[PubMed]
0149-5992
45.
Nishida
T
,
Tsuji
S
,
Tsujii
M
,
Arimitsu
S
,
Sato
T
,
Haruna
Y
, et al.
Gastroesophageal reflux disease related to diabetes: analysis of 241 cases with type 2 diabetes mellitus
.
J Gastroenterol Hepatol
.
2004
Mar
;
19
(
3
):
258
65
.
[PubMed]
0815-9319
46.
Horikawa
A
,
Ishii-Nozawa
R
,
Ohguro
M
,
Takagi
S
,
Ohtuji
M
,
Yamada
M
, et al.
Prevalence of GORD (gastro-oesophageal reflux disease) in Type 2 diabetes and a comparison of clinical profiles between diabetic patients with and without GORD
.
Diabet Med
.
2009
Mar
;
26
(
3
):
228
33
.
[PubMed]
0742-3071
47.
Yönem
Ö
,
Sivri
B
,
Özdemir
L
,
Nadir
I
,
Yüksel
S
,
Uygun
Y.
Gastroesophageal reflux disease prevalence in the city of Sivas.
The Turkish journal of gastroenterology: the official journal of Turkish Society of Gastroenterology.
2013
;24(4):303-10.
48.
Jin
HY
,
Park
TS
.
Can nerve conduction studies detect earlier and predict clinical diabetic neuropathy?
J Diabetes Investig
.
2015
Jan
;
6
(
1
):
18
20
.
[PubMed]
2040-1116
49.
Cumpston
EC
,
Blumin
JH
,
Bock
JM
.
Dual pH with multichannel intraluminal impedance testing in the evaluation of subjective laryngopharyngeal reflux symptoms
.
Otolaryngol Head Neck Surg
.
2016
Dec
;
155
(
6
):
1014
20
.
[PubMed]
0194-5998
50.
Newman
R
,
Vilardell
N
,
Clavé
P
,
Speyer
R
. Effect of bolus viscosity on the safety and efficacy of swallowing and the kinematics of the swallow response in patients with oropharyngeal dysphagia: white paper by the European Society for Swallowing Disorders (ESSD). Dyphagia.
2016
;31(2):232–49.
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