Nutrition 124 (2024) 112440

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Nutrition
journal homepage: www.nutritionjrnl.com

Applied nutritional investigation

Dysphagia risk evaluated by the Eating Assessment Tool-10 is

associated with health-related quality of life in patients with chronic
liver disease
Takao Miwa M.D. a,*, Tatsunori Hanai M.D., Ph.D. a,b, Itsuki Hayashi D.D.S. c, Sachiyo Hirata R.D. b,
Kayoko Nishimura R.D. b, Shinji Unome M.D. a, Yuki Nakahata M.D. a,d, Kenji Imai M.D., Ph.D. a,
Yohei Shirakami M.D., Ph.D. a, Atsushi Suetsugua M.D., Ph.D. a, Koji Takai M.D., Ph.D. a,e,
Masahito Shimizu M.D., Ph.D. a
a
Department of Gastroenterology/Internal Medicine, Graduate School of Medicine, Gifu University, Gifu, Japan
b
Center for Nutrition Support and Infection Control, Gifu University Hospital, Gifu, Japan
c
Department of Oral and Maxillofacial Sciences, Graduate School of Medicine, Gifu University, Gifu, Japan
d
Department of Gastroenterology, Asahi University Hospital, Gifu, Japan
e
Division for Regional Cancer Control, Graduate School of Medicine, Gifu University, Gifu, Japan

A R T I C L E I N F O A B S T R A C T

Article History: Objective: This study aimed to reveal the prevalence and characteristics of individuals at risk of dysphagia in
Received 14 February 2024 patients with chronic liver disease (CLD) and its association with health-related quality of life (HRQOL).
Received in revised form 14 March 2024 Methods: This cross-sectional study included 335 outpatients with CLD. Dysphagia risk, sarcopenia risk, mal-
Accepted 23 March 2024
nutrition risk, and HRQOL were assessed using the Eating Assessment tool-10 (EAT-10), SARC-F, Royal Free
Hospital-Nutrition Prioritizing Tool (RFH-NPT), and Chronic Liver Disease Questionnaire (CLDQ), respectively.
Keywords:
Dysphagia risk and low HRQOL were based on EAT-10 3 and CLDQ overall score <5, respectively. Factors
Frailty
associated with dysphagia risk and low HRQOL were assessed using the logistic regression model.
Liver cirrhosis
Malnutrition
Results: Dysphagia risk and lower HRQOL were observed in 10% and 31% of the patients, respectively. Patients
Oral health with dysphagia risk were older, had lower liver functional reserve, were at higher risk for sarcopenia and
Sarcopenia malnutrition, and showed lower CLDQ overall score (median, 4.41 vs. 5.69; P < 0.001) than those without.
Sarcopenic dysphagia After adjustment, SARC-F (odds ratio [OR], 1.24; 95% confidence interval [CI], 1.02
1.50; P = 0.029) and RFH-
NPT (OR, 1.71; 95% CI, 1.04
2.81; P = 0.034) scores were independently associated with dysphagia risk. EAT-
10 (OR, 1.17; 95% CI, 1.04
1.30; P = 0.008) and SARC-F (OR, 1.37; 95% CI, 1.18
1.59; P < 0.001) scores were
also independently associated with low HRQOL.
Conclusions: Dysphagia risk was prevalent in approximately 10% of patients with CLD and was associated
with a risk of sarcopenia and malnutrition. Furthermore, dysphagia risk was related to HRQOL in patients
with CLD.
© 2024 Elsevier Inc. All rights reserved.

Introduction specific populations, especially in those with musculoskeletal, neu-

Dysphagia refers to the dysfunction or deterioration of swal-
lowing and is usually a multidimensional syndrome rather than a
localized disease specific to the oropharynx [1,2]. Approximately,
8% of the global population and 20% of the older population suffer
from dysphagia, and the prevalence increases from 20% to 40% in
This research did not receive any specific grant from funding agencies in the pub-
lic, commercial, or not-for-profit sectors.
*Corresponding author. Tel.: +81-58-230-6308; fax: +81-58-230-6310.
E-mail address: miwa.takao.a6@f.gifu-u.ac.jp (T. Miwa).
rological, and otolaryngologic diseases [1,2]. Furthermore, recent
studies have focused on sarcopenia, characterized by loss of skele-
tal muscle mass and strength, as a leading cause of dysphagia [3].
Accumulated evidence has shown that dysphagia causes dehydra-
tion, malnutrition, and aspiration pneumonia, all of which worsen
the morbidity and mortality of the patients [1]. With the increasing
burden of dysphagia, its early screening and intervention are
important in daily practice; however, approximately 60% of
patients with dysphagia do not report their symptoms in routine
care [2].

https://doi.org/10.1016/j.nut.2024.112440
0899-9007/© 2024 Elsevier Inc. All rights reserved.
2 T. Miwa et al. / Nutrition 124 (2024) 112440
Chronic liver disease (CLD), as represented by cirrhosis, caused
by factors such as hepatitis virus infection, alcohol, and metabolic
abnormalities, is a major health problem worldwide. CLD is fre-
quently complicated by malnutrition and sarcopenia, and these
pathologies define the health-related quality of life (HRQOL) and
prognosis of the patients [4]. Therefore, many patients with CLD,
especially those with older age, malnutrition, and sarcopenia, can
be at high risk for complications of dysphagia. However, very few
studies have been conducted on the prevalence, clinical charac-
teristics, and impact on outcomes of dysphagia in patients with
CLD.
HRQOL is a multidimensional concept that comprehensively
reflects the physical, psychological, social, and functional condition
of illness from the patient’s perspective [5]. Regardless of etiology,
patients with CLD are known to have significantly lower HRQOL
than that of the general population [6]. Assessment of HRQOL in
clinical practice is crucial not only for understanding the burden of
disease from the patient’s perspective but also for assessing the
risk of hospitalization and mortality in patients with CLD [6]. In
general, liver functional reserves and complications of CLD, such as
malnutrition, sarcopenia, ascites, and hepatic encephalopathy, can
lead to lower HRQOL in patients with CLD [5,7,8]. However, data
on the impact of dysphagia on HRQOL in patients with CLD are lim-
ited.
We hypothesized that a certain proportion of patients with CLD
suffer from dysphagia. Additionally, similar to the roles of malnu-
trition and sarcopenia, dysphagia can impair HRQOL in these
patients. Therefore, the primary aim of this study was to reveal the
prevalence and clinical characteristics of individuals at risk of dys-
phagia using the Eating Assessment Tool-10 (EAT-10) in general
outpatients with CLD [9]. The secondary aim was to determine the
impact of dysphagia risk on HRQOL in these patients.
Material and methods
Study design and patients
This cross-sectional study evaluated 437 outpatients with CLD who arrived at
Gifu University Hospital (Gifu, Japan) from September 2022 to December 2022.
The study protocol was reviewed and approved by the Institutional Review Board
of the Graduate School of Medicine, Gifu University (approval number: 2022-179),
and the study was conducted in accordance with the Declaration of Helsinki. A
health care professional explained the study objective to the candidates and writ-
ten informed consent was obtained from all participants.
The inclusion criteria were patients with CLD of any etiology, aged 18 y. The
exclusion criteria were patients with neurological diseases, musculoskeletal dis-
eases, head or neck cancers, trauma, and primary esophageal diseases, all of which
may affect the assessment of dysphagia.
Outcomes and variables
The primary outcomes were the prevalence and clinical characteristics of
individuals at risk of dysphagia using the EAT-10 in patients with CLD. The sec-
ondary outcomes were factors affecting HRQOL in patients with CLD. Informa-
tion regarding dysphagia, sarcopenia, malnutrition, and HRQOL was collected
through questionnaires during outpatient visits. Cirrhosis was diagnosed based
on histology, biochemical parameters, imaging, and clinical symptoms.
Patients’ clinical characteristics and laboratory data were assessed on the day
of enrollment. Liver functional reserves were evaluated using the Child
Pugh,
model for end-stage liver disease (MELD), and albumin-bilirubin (ALBI) scores
[10
12]. Hepatic encephalopathy and hepatocellular carcinoma assessment
were evaluated based on the West Haven criteria and Japanese guidelines,
respectively [13,14].
Assessment of dysphagia risk
Dysphagia risk was evaluated using the EAT-10 questionnaire which consists
of 10 items [9]. Each item was scored from 0 (no problem) to 4 (severe problem)
points, and the total score was calculated. A total EAT-10 score of 3 was assessed
as patients at risk of dysphagia based on a pre-evaluated cutoff value [15]. The reli-
ability of EAT-10 3 for evaluating dysphagia has been established by a previous
meta-analysis that showed a sensitivity of 0.87, specificity of 0.82, and area under
the curve of 0.90, using video fluoroscopic swallowing test and flexible endoscopic
evaluation of swallowing as reference data [15].
Assessment of HRQOL
HRQOL was assessed using the Chronic Liver Disease Questionnaire (CLDQ),
invented to assess disease-specific HRQOL in patients with CLD [16,17]. The
CLDQ is a self-administrated questionnaire consisting of 29 items, each of
which is answered on a 7-point scale from 1 (worst) to 7 (best). The mean score
for all items was assessed as overall HRQOL and subdomains including fatigue,
abdominal symptoms, systemic symptoms, activity, emotional function, and
worry were also evaluated. A higher CLDQ score indicated less frequent symp-
toms and better HRQOL [16,17]. A CLDQ overall score <5 was determined as
having low HRQOL [6].
Assessment of sarcopenia and malnutrition risks
The risk of sarcopenia was assessed using the SARC-F questionnaire, recom-
mended by the European Working Group on Sarcopenia in Older People [18,19].
Patients with SARC-F 4 were considered as being at risk of sarcopenia based on
previous reports [18,20]. The risk of malnutrition was assessed using the Royal
Free Hospital-Nutrition Prioritizing Tool (RFH-NPT), recommended by the Euro-
pean Association for the Study of the Liver [21,22]. Patients with RFH-NPT 1
were classified as being at risk of malnutrition [21].
Sample size calculation
A minimum of 70 outcomes were necessary for the multivariate analysis
including seven variables (age, sex, liver functional reserves, dysphagia, sarcope-
nia, malnutrition, and enteral nutrition). Given an estimated 20% prevalence of
low HRQOL among patients with CLD, we calculated a required sample size of 350
to evaluate the association between HRQOL and dysphagia risk in our study.
Statistical methods
Numeric parameters were represented as medians (interquartile ranges),
while categorical parameters were expressed as counts (percentages). The differ-
ences between the groups were assessed using either the Mann
Whitney U test,
Kruskal
Wallis test, or chi-squared test. Factors associated with dysphagia risk
and low HRQOL were evaluated using logistic regression analysis and the results
were presented as odds ratios (ORs), accompanied by 95% confidence intervals
(CIs). Multivariate analyses included the priori selected factors considering the
clinical relevance and the Child
Pugh score in model 1, MELD score in model 2,
and ALBI score in model 3. For all analyses, the P-values reported were two-tailed,
and statistical significance was established at a threshold of <0.05. All analyses
were performed using JMP Pro (version 17.0.0, SAS Institute Inc., Cary, NC, USA)
and R (version 4.1.3, R Foundation for Statistical Computing, Vienna, Austria).
Results
Clinical characteristics of the enrolled patients with CLD
Of the 437 outpatients with CLD, 102 were excluded from the
study, and the remaining 335 patients were included in the analy-
sis (Supplementary Fig. 1). The clinical characteristics of the
enrolled patients are shown in Table 1. The median age of the pop-
ulation was 66 y, and 50% were male. Hepatitis B (35%) was the
main etiology of CLD followed by hepatitis C (25%), metabolic dys-
function-associated steatohepatitis (9%), alcohol-related liver dis-
ease (7%), and others (24%). Cirrhosis was observed in 30% of the
patients. In complications, ascites, hepatic encephalopathy, and
hepatocellular carcinoma were present in 5%, 2%, and 8% of the
patients, respectively. None of the patients were receiving paren-
teral nutrition; however, 3% were on enteral nutrition. The median
Child
Pugh, MELD, and ALBI scores were 5, 6, and -2.83, respec-
tively. The patients with dysphagia, at risk of sarcopenia, and risk
of malnutrition were 33 (10%), 51 (15%), and 68 (20%), respectively.
The median CLDQ overall score was 5.55, and 103 (31%) were diag-
nosed with low HRQOL based on a CLDQ overall score <5.
A comparison of patients with and without dysphagia risk is
also shown in Table 1. Patients with EAT-10 3 were older and had
more advanced CLD in terms of cirrhosis, hepatic encephalopathy,
 T. Miwa et al. / Nutrition 124 (2024) 112440 3

Table. 1
Baseline characteristics of patients with CLD divided by dysphagia risk

Characteristic All patients (n = 335) EAT-10 <3 (n = 302) EAT-10 3 (n = 33) P-value*

Age (y) 66 (44
75) 65 (54
74) 76 (63
81) 0.001

Male, n (%) 169 (50) 153 (51) 16 (48) 0.812
Body mass index (kg/m2) 23.1 (21.0
25.3) 23.1 (21.2
25.0) 22.5 (19.6
25.2) 0.417
Etiology of CLD, n (%) 0.647
HBV 116 (35) 106 (35) 10 (30)
HCV 83 (25) 73 (24) 10 (30)
ALD 25 (7) 22 (7) 3 (9)
MASH 31 (9) 30 (10) 1 (3)
Others 80 (24) 71 (24) 9 (27)
Diabetes mellitus, n (%) 62 (19) 59 (20) 3 (9) 0.142
Ascites, n (%) 17 (5) 14 (5) 3 (9) 0.228
Hepatic encephalopathy, n (%) 8 (2) 5 (2) 3 (9) 0.008
Hepatocellular carcinoma, n (%) 27 (8) 24 (8) 3 (9) 0.819
Liver cirrhosis, n (%) 99 (30) 81 (27) 18 (55) 0.002
Enteral nutrition, n (%) 9 (3) 5 (2) 4 (12) <0.004
Child
Pugh score 5 (5
5) 5 (5
5) 5 (5
7) <0.001
Child
Pugh class (A/B/C), n 311/20/4 287/12/3 24/8/1 <0.001
MELD score 6 (8
8) 6 (6
8) 6 (6
9) 0.450
ALBI score -2.83 (-3.04
-2.57) -2.84 (-3.07
-2.60) -2.70 (-2.99
-1.53) 0.010
International normalized ratio 1.00 (0.95
1.00) 1.00 (0.95
1.00) 1.00 (0.97
1.02) 0.500
Platelet (109/L) 185 (140
237) 187 (146
243) 135 (100
200) 0.001
Creatinine (mg/dL) 0.78 (0.65
0.93) 0.77 (0.65
0.92) 0.80 (0.65
1.01) 0.492
Albumin (g/dL) 4.2 (3.9
4.5) 4.3 (4.0
4.5) 4.0 (3.4
4.3) <0.001
Bilirubin (mg/dL) 0.8 (0.6
1.1) 0.8 (0.6
1.1) 0.8 (0.6
1.2) 0.821
Sodium (meq/L) 140 (138
141) 140 (138
141) 140 (138
141) 0.941
SARC-F 4, n (%) 51 (15) 39 (13) 12 (36) <0.001
RFH-NPT 1, n (%) 68 (20) 15 (45) 53 (18) <0.001
CLDQ overall score 5.55 (4.86
6.34) 5.69 (4.97
6.41) 4.41 (3.50
5.17) <0.001
Fatigue 4.60 (3.80
5.80) 4.80 (4.00
5.80) 3.60 (2.70
4.10) <0.001
Abdominal symptom 6.00 (4.67
6.67) 6.00 (4.92
6.67) 4.33 (3.67
5.50) <0.001
Systemic symptoms 5.80 (5.00
6.60) 6.00 (5.20
6.60) 4.80 (4.10
5.70) <0.001
Activity 6.00 (5.00
7.00) 6.33 (5.33
7.00) 5.00 (4.33
5.67) <0.001
Emotional function 5.63 (4.63
6.50) 5.75 (4.75
6.63) 4.25 (3.63
5.31) 0.020
Worry 6.00 (5.00
7.00) 6.20 (5.20
7.70) 4.40 (3.40
5.70) 0.020
ALBI, albumin-bilirubin; ALD, alcohol-related liver disease; CLD, chronic liver disease; CLDQ, Chronic Liver Disease Questionnaire; EAT-10, Eating Assessment Tool-10; HBV,
hepatitis B virus; HCV, hepatitis C virus; MASH, metabolic dysfunction-associated steatohepatitis; MELD, model for end-stage liver disease; RFH-NPT, Royal Free Hospital-
Nutritional Prioritizing Tool.
Values are presented as number (percentage) or median (interquartile range).
*Statistical differences between the two groups were analyzed using the chi-square test or Mann
Whitney U test.

serum albumin levels, platelet count, Child-Pugh, MELD, and ALBI
scores than those with EAT-10 <3. Furthermore, patients with
EAT-10 3 were characterized by significantly worse CLDQ overall
score (median, 4.41 vs. 5.69; P < 0.001), SARC-F, and RFH-NPT than
that of those with EAT-10 <3. In other words, patients with older
age (14% vs. 6%, P = 0.024, Fig. 1A), cirrhosis (18% vs. 6%, P = 0.002,
Fig. 1B), at risk of malnutrition (22% vs. 7%, P < 0.001, Fig. 1C), and
at risk of sarcopenia (24% vs. 7%, P < 0.001, Fig. 1D) had signifi-
cantly higher prevalence of EAT-10 3 than in those without.
Impact of risks of sarcopenia and malnutrition on dysphagia risk in
patients with CLD
Regarding factors associated with dysphagia risk, multivariate
model 1 including the Child
Pugh score showed that SARC-F (OR,
1.24; 95% CI, 1.02
1.50; P = 0.029) and RFH-NPT (OR, 1.71; 95% CI,
1.04
2.81; P = 0.034) were independently associated with dyspha-
gia risk (EAT-10 3) in patients with CLD. The results were also
confirmed in model 2 including the MELD score and model 3
including the ALBI score instead of the Child
Pugh score in model
1 (Table 2). The detail of the multivariate analyses is shown in Sup-
plementary Table 1. Among patients with data available for the
Global Leadership Initiative on Malnutrition criteria and muscle
mass (n = 173), malnutrition was associated with an increased risk
of dysphagia in patients with CLD (Supplementary Table 2) [23,24].
Impact of the EAT-10 score on HRQOL in patients with CLD
Regarding factors associated with HRQOL, multivariate model 1
including the Child
Pugh score showed that EAT-10 (OR, 1.17;
95% CI, 1.04
1.30; P = 0.008) and SARC-F (OR, 1.37; 95% CI,
1.18
1.59; P < 0.001) were independently associated with low
HRQOL (CLDQ overall score <5) in patients with CLD. The impact
of EAT-10 on HRQOL reduction was similar in the results of analy-
ses of model 2 including the MELD score and model 3 including
the ALBI score instead of the Child
Pugh score in model 1 (Table 3).
The detail of the multivariate analyses is shown in Supplementary
Table 3. The association between HRQOL and EAT-10 was also sig-
nificant among patients with data available for the Global Leader-
ship Initiative on Malnutrition criteria and muscle mass (n = 173)
(Supplementary Table 4) [23,24].
Association between the risks of dysphagia and sarcopenia in patients
with CLD
To evaluate the association between the risks of dysphagia and
sarcopenia in patients with CLD, patients were divided into four
groups based on the presence of EAT-10 3 and SARC-F 4
(Fig. 2A). The results showed that 79% (n = 263) had neither EAT-
10 3 nor SARC-F 4, 12% (n = 39) had only SARC-F 4, 6% (n = 21)
had only EAT-10 3, and 4% (n = 12) had both EAT-10 3 and
SARC-F 4 (4%). The median CLDQ overall scores for patients with
none of the risk factors, SARC-F 4 only, EAT-10 3 only, and both
4 T. Miwa et al. / Nutrition 124 (2024) 112440

Fig. 1. The prevalence of individuals at risk of dysphagia (EAT-10 3) in patients with chronic liver disease. The prevalence of individuals at risk of dysphagia was compared
between patients (A) aged 65 and <65 y, (B) with and without cirrhosis, (C) with RFH-NPT 1 and 0, and (D) with SARC-F 4 and <0. EAT-10, Eating Assessment Tool-10;
RFH-NPT, Royal Free Hospital-Nutritional Prioritizing Tool.

EAT-10 3 and SARC-F 4 were 5.79, 5.14, 4.62, and 3.98, respec-
tively (P < 0.001; Fig. 2B). Of note, patients with EAT-10 3 alone
displayed significantly lower CLDQ overall score than in those with
SARC-F 4 alone (P = 0.040).
Discussion
Since more than half of the patients with dysphagia do not
report their symptoms, little has been done to investigate the prev-
alence and clinical relevance of dysphagia in patients with CLD. The
first integrating finding of the present study was that 10% of outpa-
tients with CLD were at risk of dysphagia assessed by EAT-10 3. In
addition, dysphagia risk was adversely affected by the risks of mal-
nutrition and sarcopenia. The second finding was that dysphagia
risk is associated with HRQOL in patients with CLD. Our results
highlight the importance of dysphagia because dietary intake is
important to maintain nutritional status and because of its robust
association with low HRQOL in patients with CLD.
In the present study including patients with CLD, the preva-
lence of individuals at risk of dysphagia was 14% among patients
aged 65 y. Since the prevalence in community-dwelling Japanese
or Chinese populations of the same age group was approximately
6% [25,26], it is likely that patients with CLD are more prone to dys-
phagia complications. Our results are supported by a previous
study of patients with cirrhosis, which showed that those with
EAT-10 3 are 7% of the total population and 13% of those aged
65 y [27]. Furthermore, the present study revealed that the prev-
alence of patients at risk of dysphagia is significantly higher in
those with cirrhosis (18%) than in those without cirrhosis (6%).
These results imply that patients with CLD, especially those with
cirrhosis, can be a high-risk population for dysphagia as other
major predisposing conditions for dysphagia such as musculoskel-
etal, neurological, and otolaryngologic diseases.
The results of the present study clearly demonstrated that the
risk of malnutrition (RFH-NPT) was independently associated with
dysphagia risk in patients with CLD. In particular, the patients with
RFH-NPT 1 had a significantly higher prevalence of patients at risk
 T. Miwa et al. / Nutrition 124 (2024) 112440 5

Table. 2 Table. 3
Impact of risks of sarcopenia and malnutrition on dysphagia risk in patients with Impact of the EAT-10 score on low HRQOL in patients with CLD
CLD
Characteristic OR (95% CI) P-value*
Characteristic OR (95% CI) P-value* y
Model 1
Model 1y Child
Pugh score 1.17 (0.79
1.73) 0.420
Child
Pugh score 0.95 (0.60
1.51) 0.837 SARC-F 1.37 (1.18
1.59) <0.001
SARC-F 1.24 (1.02
1.50) 0.029 RFH-NPT 1.36 (0.89
2.07) 0.158
RFH-NPT 1.71 (1.04
2.81) 0.034 EAT-10 1.17 (1.04
1.30) 0.008

Model 2z Model 2z
MELD score 1.00 (0.88
1.13) 0.954 MELD score 1.02 (0.95
1.09) 0.594
SARC-F 1.23 (1.02
1.49) 0.045 SARC-F 1.38 (1.19
1.61) <0.001
RFH-NPT 1.68 (1.06
2.68) 0.029 RFH-NPT 1.41 (0.94
2.12) 0.099
EAT-10 1.16 (1.04
1.29) 0.009
Model 3x
ALBI score 0.87 (0.32
2.36) 0.780 Model 3x
SARC-F 1.24 (1.02
1.50) 0.029 ALBI score 1.49 (0.76
2.95) 0.247
RFH-NPT 1.72 (1.05
2.81) 0.031 SARC-F 1.36 (1.17
1.59) <0.001
RFH-NPT 1.32 (0.87
2.02) 0.193
ALBI, albumin-bilirubin; CI, confidence interval; CLD, chronic liver disease; MELD,
EAT-10 1.16 (1.04
1.29) 0.009
model for end-stage liver disease; OR, odds ratio; RFH-NPT, Royal Free Hospital-
Nutritional Prioritizing Tool. ALBI, albumin-bilirubin; CI, confidence interval; CLD, chronic liver disease; EAT-10,
*Multivariate analyses were performed using the logistic regression model. Eating Assessment Tool-10; HRQOL, health-related quality of life; MELD, model for
y
Model 1 included age, sex, presence of cirrhosis, Child
Pugh score, SARC-F, RFH- end-stage liver disease; OR, odds ratio; RFH-NPT, Royal Free Hospital-Nutritional
NPT, and enteral nutrition. Prioritizing Tool.
z
Model 2 included age, sex, presence of cirrhosis, MELD score, SARC-F, RFH-NPT, and *Multivariate analyses were performed using the logistic regression model.
y
enteral nutrition. Model 1 included age, sex, presence of cirrhosis, Child
Pugh score, SARC-F, RFH-
x
Model 3 included age, sex, presence of cirrhosis, ALBI score, SARC-F, RFH-NPT, and NPT, EAT-10, and enteral nutrition.
z
enteral nutrition. Model 2 included age, sex, presence of cirrhosis, MELD score, SARC-F, RFH-NPT,
EAT-10, and enteral nutrition.
x
Model 3 included age, sex, presence of cirrhosis, ALBI score, SARC-F, RFH-NPT, EAT-
of dysphagia than those with RFH-NPT 0 (22 vs. 7%). In general, mal-
10, and enteral nutrition.
nutrition critically impairs the nutritional status of older adults
[28,29]. A recent meta-analysis has shown that older adults with
dysphagia have a twofold increased risk of malnutrition than those sarcopenia in patients with cirrhosis [27]. However, the prior work
without dysphagia [29]. It is well-known that malnutrition has a sig- was limited by a small sample size [27]. Therefore, our results
nificant impact on the prognosis of patients with CLD [30]. There- strengthen the evidence of the association between dysphagia and
fore, if dysphagia is identified as a potential cause of malnutrition in sarcopenia in patients with CLD. Our results are also supported by
patients with CLD, early screening, and intervention should be con- several geriatric communities which emphasized that dysphagia is
sidered to improve the nutritional status of the patients. a geriatric syndrome and has a robust association between sys-
The risk of sarcopenia (SARC-F) was also independently associ- temic sarcopenia in various populations [3,31]. Of note, some
ated with dysphagia risk in patients with CLD. A previous study patients in the present study were at risk for both dysphagia and
has suggested the association between EAT-10 score and sarcopenia, while others had only one or none of them. This seems

Fig. 2. The association between dysphagia risk (EAT-10 3) and sarcopenia risk (SARC-F 4) in patients with chronic liver disease. (A) The patients were divided into four
groups according to dysphagia risk and sarcopenia risk. (B) The CLDQ overall score is according to the four subgroups. CLDQ, chronic liver disease questionnaire; EAT-10, Eat-
ing Assessment Tool-10.
6 T. Miwa et al. / Nutrition 124 (2024) 112440
reasonable because the association between dysphagia and sarco-
penia has been explained by two types of clinical course: sarcope-
nia followed by dysphagia and dysphagia followed by sarcopenia/
malnutrition [3].
Another integrating finding of the present study is that dyspha-
gia risk was associated with HRQOL in patients with CLD. Notably,
even though this study included outpatients with CLD who had rel-
atively preserved liver functional reserves, almost one-third of
them had low HRQOL (CLDQ overall score <5). The results of multi-
variate analyses accounting for confounding of cirrhosis, liver func-
tional reserves, and risks of malnutrition and sarcopenia showed
that risks of dysphagia and sarcopenia were robust factors that are
associated with HRQOL in patients with CLD. Furthermore, a sub-
group analysis between dysphagia risk alone and sarcopenia risk
alone revealed that dysphagia risk alone had a stronger impact on
HRQOL than did sarcopenia risk alone. These results are also sup-
ported by a previous study showing that dysphagia impairs HRQOL
in older adults [32]. The results of this study imply that interven-
tions for dysphagia and its risk factors, such as sarcopenia and mal-
nutrition, may improve HRQOL in patients with CLD. However,
evidence regarding the treatment of dysphagia and its effects on
systemic conditions are limited [33]. Therefore, further studies are
expected to evaluate the clinical relevance of dysphagia and its
treatment in patients with CLD.
There are some limitations to be addressed in this study. First,
this was a single-center study including a limited sample size. Sec-
ond, this study did not use gold-standard diagnostic tools for the
diagnosis of dysphagia, sarcopenia, and malnutrition. In fact, the
statistical power in the association between muscle mass and dys-
phagia risk was negative in the subgroup analysis. Therefore,
future studies are required to confirm the results of our study using
gold-standard diagnostic tools for dysphagia, malnutrition, and
sarcopenia. Despite these limitations, our study has several
strengths, including a large number of participants and a compre-
hensive assessment of dysphagia, sarcopenia, and malnutrition
risk using different multivariate models to strengthen the evi-
dence. Since dysphagia is a multifactorial disorder influenced by
aging, malnutrition, sarcopenia, and inflammation [34], a compre-
hensive assessment and a multidisciplinary team are important for
managing dysphagia and improving HRQOL in patients with CLD.
Conclusions
In conclusion, approximately 10% of patients with CLD were at
risk of dysphagia. Furthermore, dysphagia risk was associated with
low HRQOL in patients with CLD. As dysphagia risk is associated
with HRQOL in patients with CLD, screening of dysphagia should
be considered in daily practice to improve the well-being of these
patients.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared to
influence the work reported in this paper.
CRediT authorship contribution statement
Takao Miwa: Writing
original draft, Methodology, Formal
analysis, Data curation, Conceptualization. Tatsunori Hanai: Writ-
ing
review & editing, Supervision, Data curation, Conceptualiza-
tion. Itsuki Hayashi: Writing
review & editing, Supervision,
Conceptualization. Sachiyo Hirata: Writing
review & editing,
Data curation. Kayoko Nishimura: Writing
review & editing,
Data curation. Shinji Unome: Writing
review & editing, Data
curation. Yuki Nakahata: Writing
review & editing, Data cura-
tion. Kenji Imai: Writing
review & editing, Data curation. Yohei
Shirakami: Writing
review & editing, Data curation. Atsushi
Suetsugua: Writing
review & editing, Data curation. Koji Takai:
Writing
review & editing, Data curation. Masahito Shimizu:
Writing
review & editing, Supervision, Data curation.
Data statement
The datasets generated and/or analyzed during the current
study are available from the corresponding author upon reason-
able request.
Acknowledgments
We would like to thank Maki Moriya for collecting the data in
this study.
Supplementary materials
Supplementary material associated with this article can be
found in the online version at doi:10.1016/j.nut.2024.112440.
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