Development, Reliability, and Validity of A Diagnostic

© 2017 The Authors. Journal of Cachexia, Sarcopenia and Muscle ‐ Clinical Reports published on
behalf of the Society on Sarcopenia, Cachexia and Wasting Disorders. This is an open‐access article
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source are credited.

Development, reliability, and validity of a diagnostic
algorithm for sarcopenic dysphagia

Takashi Mori1, Ichiro Fujishima2, Hidetaka Wakabayashi3, Fumiko Oshima4, Masataka Itoda5, Kenjiro Kunieda2, Jun
Kayashita6, Shinta Nishioka7, Akiko Sonoda8, Yoshitoshi Kuroda9, Minoru Yamada10, Sumito Ogawa11

1 Department of Oral and Maxillofacial Surgery, Southern Tohoku General Hospital, 7‐115, Yatsuyamada, Koriyama‐shi, Fukushima, 963‐8563,
Japan; 2 Hamamatsu City Rehabilitation Hospital, 1‐6‐1, Wagokita, Naka‐ku Hamamatsu‐shi, Shizuoka, 433‐8511, Japan; 3 Department of
Rehabilitation Medicine, Yokohama City University Medical Center, 4‐57 Urafune‐chou, Minami ward, Yokohama‐shi, Japan; 4 Department of
Neurology, Japanese Red Cross Kyoto Daiichi Hospital, 15‐749, Hommachi, Higashiyama‐ku Kyoto‐shi, Kyoto, 605‐0981, Japan; 5 Wakakusa‐Tatsuma
Rehabilitation Hospital, 1580, Tatsuma, Daito‐shi, Osaka, 574‐0012, Japan; 6 Department of Health Sciences, Faculty of Human Culture and Science,
Prefectural University of Hiroshima, 1‐1‐71,usihnahigasi, Miami‐ku, Hiroshima‐shi, Hiroshima, 734‐8558, Japan; 7 Department of Clinical Nutrition
and Food Services, Nagasaki Rehabilitation Hospital, 4‐11, Ginyacho, Nagasaki‐shi, Nagasaki, 850‐0854, Japan; 8 Department of Audiology and
Logopedics, Japan Collage of Rehabilitation and Welfare Professionals, 2‐14, Wakamiyacho, Nakamura‐ku Nagoya‐shi, Aichi, 453‐0023, Japan; 9
Department of Rehabilitation, St. Francis Hospital, 9‐20, Kominemachi, Nagasaki‐shi, Nagasaki, 852‐8125, Japan; 10 Graduate School of
Comprehensive Human Sciences, University of Tsukuba, 3‐29‐1, Otsuka, Bunkyo‐ku, Tokyo, 112‐0012, Japan; 11 Department of Geriatric Medicine,
Graduate School of Medicine, The University of Tokyo, 7‐3‐1, Hongo, Bunkyo‐ku, Tokyo

Abstract

Background Sarcopenic dysphagia is characterized by difficulty swallowing due to loss of whole‐body skeletal and
swallowing muscle mass and function. Despite multiple reports regarding sarcopenic dysphagia, no verified diagnostic
methods exist. The purpose of this study was to develop a diagnostic algorithm for sarcopenic dysphagia and verify its
reliability and validity.

Methods First, our research group, the Working Group on Sarcopenic Dysphagia, developed a diagnostic algorithm for
sarcopenic dysphagia. Patients 65 years and older who could follow commands were eligible for assessment using the
algorithm. Patients without whole‐body sarcopenia, with normal swallowing function, and with a disease that was an
obvious cause of their dysphagia were considered not to have sarcopenic dysphagia. Then, swallowing muscle
strength was assessed by tongue pressure. Those with poor swallowing muscle strength were deemed to be at
probable risk for sarcopenic dysphagia and those with normal swallowing muscle strength to be at possible risk for
sarcopenic dysphagia. Second, we applied the algorithm to inpatients 65 years and older and investigated their
characteristics, muscle mass, muscle strength, motor function, swallowing muscle strength, swallowing function, and
nutritional status. We investigated the reliability of the algorithm by analyzing intra‐ and inter‐class correlation
coefficients using kappa statistics. Third, we investigated the validity of the algorithm by analyzing the difference in
the proportion of patients with sarcopenic dysphagia between the no malnutrition and malnutrition groups and
investigated the risk factors for sarcopenic dysphagia using logistic regression analysis.

Results A total of 119 patients participated in this study. Their mean age was 86.1 years, and 55 (46%) were men.
Among the 119 patients, 32 were categorized as having possible sarcopenic dysphagia, 18 probable sarcopenic
dysphagia, and 69 no sarcopenic dysphagia. The intra‐class coefficient for the algorithm was 0.87 (95% confidence
interval [CI]: 0.731.01), and the inter‐class coefficient was 0.98 (95% CI: 0.921.02), indicating high intra‐ and inter‐
rater reliabilities. In the investigation of the algorithm’s validity, 67 patients were analyzed. The proportion of patients
with sarcopenic dysphagia was significantly higher in the malnutrition than in the no malnutrition group (P = 0.028).
Malnutrition and age were independently associated with sarcopenic dysphagia (P = 0.013 and 0.003, respectively).

Conclusions A diagnostic algorithm for sarcopenic dysphagia was developed, and its reliability and validity were
verified. All older patients with sarcopenia or dysphagia should be assessed for sarcopenic dysphagia, which requires
treatment involving not only rehabilitation for dysphagia but also nutritional improvement.

Address for correspondence: Wakabayashi Hidetaka, Department of Rehabilitation Medicine, Yokohama City University Medical Center, 4‐57
Urafune‐chou, Minami‐ku, Yokohama‐shi, Japan 232‐0024 , Phone: +81‐45‐261‐5656, Fax: +81‐45‐253‐9955, E‐mail: noventurenoglory@gmail.com
Keywords: Dysphagia, Sarcopenia, Nutrition, Diagnosis, Algorithm, Reliability
Received 27 December 2016 Accepted 12 April 2017
Journal of Cachexia, Sarcopenia and Muscle ‐ Clinical Reports| Volume 2| Issue 2|e00017|Page 1

Development, reliability, and validity of a diagnostic algorithm for sarcopenic dysphagia

Introduction [11] following cancers and heart diseases. Moreover,

sarcopenic dysphagia is both the cause and the result of
Sarcopenic dysphagia is a novel concept aspiration pneumonia [1]. Furthermore, people with
characterized by difficulty swallowing because of the loss severe dysphagia who are not able to manage the oral
of whole‐body skeletal and swallowing muscle mass and intake of food have a lower quality of life attributable to
function [1‐3]. The presence of dysphagia and whole‐ loss of the pleasure of eating. Therefore, the
body sarcopenia are necessary diagnostic criteria for management of sarcopenic dysphagia is an important
sarcopenic dysphagia, but these are not sufficient criteria current and future public health issue, and further
(Table 1) [1]. Most individuals with dysphagia and loss of advances in this area are required [12].
swallowing muscle mass and function have whole‐body The association between sarcopenia and
sarcopenia and thus may be diagnosed with sarcopenic dysphagia has been investigated. Age‐related loss of the
dysphagia. In contrast, those with loss of swallowing muscle mass involved in swallowing, such as a decrease
muscle mass or muscle power without whole‐body in tongue thickness [13], the geniohyoid muscle [14], and
sarcopenia are not diagnosed with sarcopenic dysphagia, the pharyngeal lumen size [15] has been reported.
because this condition occurs only in patients with other Decreased tongue pressure [16‐18] and head lifting
neuromuscular diseases such as myositis and strength [19] are associated with dysphagia. Loss of
amyotrophic lateral sclerosis. Causes of sarcopenia are whole‐body muscle mass [20‐24] and hand grip strength
age, inactivity, malnutrition, and diseases including [25, 26] are associated with dysphagia. Furthermore,
invasion (acute inflammation), cachexia (chronic whole‐body sarcopenia is a risk factor for dysphagia in
inflammation), and neuromuscular diseases [4]. We older individuals [5, 27, 28]. Moreover, sarcopenic
determined that neuromuscular disease‐related dysphagia may occur in stroke patients with a severe risk
sarcopenia is not included among the causes of of malnutrition, independently of neurological deficits
sarcopenic dysphagia, because dysphagia due to [29]. These results indicate the importance of sarcopenic
neuromuscular diseases appears to be a separate dysphagia, although evidence for this condition is
category from sarcopenic dysphagia. Dysphagic patients limited.
with age‐, activity‐, nutrition‐, invasion‐, cachexia‐related The prevalence of sarcopenic dysphagia has not
sarcopenia of the whole‐body and swallowing muscle, in been reported, because no firm diagnostic criteria exist
whom the main cause of dysphagia is sarcopenia, but not for this condition. At the symposium of the 19th Annual
neuromuscular diseases, are diagnosed with sarcopenic Meeting of the Japanese Society of Dysphagia
dysphagia. Rehabilitation, a consensus was reached on the proposed
Whole‐body sarcopenia is likely to occur prior to diagnostic criteria for sarcopenic dysphagia (Table 1) [1].
sarcopenic dysphagia. Maeda et al [5] reported that Some case reports concerning treatment of sarcopenic
among patients without dysphagia, 68.8% have dysphagia have used these diagnostic criteria [7, 30];
sarcopenia with a mean appendicular skeletal muscle however, the reliability and validity have not been
index lower than the cutoff value reported by the Asian verified. Developing reliable and valid diagnostic criteria
Working Group for Sarcopenia (AWGS) [6]. In contrast, for sarcopenic dysphagia is fundamental to conducting
95.5% of patients with dysphagia have sarcopenia [5], research and improving the management of this
suggesting that whole‐body sarcopenia precedes condition in clinical practice.
sarcopenic dysphagia. Moreover, a patient with The purpose of this study was to develop a
sarcopenic dysphagia after lung cancer surgery exhibited diagnostic algorithm for sarcopenic dysphagia and verify
restored normal swallowing function, while whole‐body its reliability and validity.
sarcopenia persisted [7]. Therefore, whole‐body
sarcopenia should be included among the diagnostic Methods
criteria for sarcopenic dysphagia.
Sarcopenia and dysphagia are common in older A cross‐sectional study was performed in a
people, especially in those over the age of 75 years. convenient sample of patients who had been admitted to
According to the International Sarcopenia Initiative, the acute‐care hospitals, convalescent rehabilitation
prevalence of sarcopenia was 1%–33% in older hospitals, and long‐term care hospitals between May
individuals [8]. The prevalence of dysphagia has been 2015 and January 2016. Eligible patients were aged 65
reported to range between 11%–68% in older individuals years and older, recommended to undergo a dysphagia
[2]. Older patients with oropharyngeal dysphagia often assessment or rehabilitation, able to answer the
have whole‐body sarcopenia [9]. Diminished chewing questionnaire, and provided written informed consent.
ability and dysphagia are common among older Asian Excluded patients were those for whom participation
patients with sarcopenia [10]. The diagnosis of was deemed inappropriate by doctors because of
sarcopenic dysphagia is important because dysphagia aggravated general conditions, consciousness
increases the risk of related complications such as disturbance, and/or severe dementia. The Ethics
aspiration pneumonia, choking, dehydration, and Committee of the Hamamatsu City Rehabilitation
malnutrition. Pneumonia, mainly aspiration pneumonia, Hospital approved the study. All patients provided
in older adults is the third leading cause of death in Japan written informed consent prior to enrollment.

A diagnostic algorithm for sarcopenic dysphagia criteria [4] when developing a diagnostic algorithm for
(Figure 1) was developed by the Working Group on sarcopenic dysphagia. We divided the diagnosis of
Sarcopenic Dysphagia, which is comprised of sarcopenic dysphagia into three categories as follows:
multidisciplinary experts and researchers of dysphagia probable sarcopenic dysphagia, possible sarcopenic
and sarcopenia, including doctors specialized in dysphagia, and no sarcopenic dysphagia. We did not
rehabilitation, neurology, geriatrics, and dentistry, include the category of definite sarcopenic dysphagia,
speech therapists, dieticians and physical therapists. because of difficulties encountered with measuring
Several meetings were conducted from September 2013 swallowing muscle mass and determining a cutoff value
to February 2016. We referenced the Consensus of swallowing muscle mass, which had not been
Diagnostic Criteria for Sarcopenic Dysphagia [1], the established by the time of the study. Diagnosing definite
Consensus Report of the AWGS [6], and the European sarcopenic dysphagia without assessing the swallowing
Working Group on Sarcopenia in Older People (EWGSOP) muscle mass should be avoided.

Table 1 Consensus diagnostic criteria for sarcopenic dysphagia
1) Presence of dysphagia.
2) Presence of whole‐body sarcopenia (generalized loss of skeletal muscle mass and strength).
3) The results of imaging tests (computed tomography, magnetic resonance imaging, ultrasonography) are consistent with a loss of swallowing
muscle mass.
4) The causes of dysphagia are excluded except for sarcopenia.
5) The main cause of dysphagia is considered to be sarcopenia (if other causes of dysphagia such as stroke, brain injury, neuromuscular
diseases, head and neck cancer, and connective tissue diseases exist).
Definite diagnosis: 1, 2, 3, 4
Probable diagnosis: 1, 2, 4
Possible diagnosis：1, 2, 5

Figure 1 Diagnostic algorithm for sarcopenic dysphagia
a) Cutoff values for hand grip strength (26 kg for men and 18 kg for women) and usual gait speed (0.8 m/s).
2
b) Cutoff values for muscle mass: calf circumference, 34 cm for men and 33 cm for women; general muscle mass (measured by DXA), 7.0 kg/m for
2 2 2
men and 5.4 kg/m for women; general muscle mass (measured by BIA), 7.0 kg/m for men and 5.7 kg/m for women
c) Cutoff values for swallowing muscle strength: 20 kPa tongue pressure.


Patients 65 years and older who could follow pressure was measured three times, and the maximum
commands were eligible to be assessed using the data were recorded. We set a cutoff value for low
algorithm because the assessment of sarcopenia using swallowing muscle strength of less than 20 kPa tongue
the EWGSOP criteria was limited to patients aged 65 pressure, because the mean tongue pressures reported
years and older [4] and following commands is necessary in older individuals with and without dysphagia are 14.7
when using the algorithm. People without whole‐body kPa and 25.3 kPa, respectively [18]. People with low
sarcopenia assessed using the AWGS criteria and who swallowing muscle strength are judged as being at
had normal swallowing function were judged as not probable risk for sarcopenic dysphagia, and people with
having sarcopenic dysphagia. We used cutoff values for normal swallowing muscle strength are judged as being
muscle strength measurements when assessing hand at a possible risk for sarcopenic dysphagia, because they
grip strength (<26 kg for men and <18 kg for women) and have dysphagia without an obvious causative disease.
for usual gait speed (<0.8 m/s), both of which were The patients’ characteristics, including age, sex,
values recommended by the AWGS criteria [6]. disease history, severity of dysphagia, nutritional status,
Appendicular muscle mass divided by height squared and results from the diagnostic algorithm for sarcopenic
(dual X‐ray absorptiometry [DXA]: 7.0 kg/m2 for men and dysphagia were examined. The severity of dysphagia was
5.4 kg/m2 for women; bioimpedance analysis [BIA]: 7.0 assessed using the Food Intake Level Scale [34], which is
kg/m2 for men and 5.7 kg/m2 for women) was used for a 10‐point observer‐rated scale that measures the
assessing low general muscle mass [6]. In cases when severity of dysphagia, from most severe (Level 1) to least
DXA and BIA were not available, we used calf severe (normal oral intake; Level 10). More specifically,
circumference for general muscle mass measurements Levels 1 to 3 relate to various degrees of non‐oral
with cutoff values (<34 cm for men and <33 cm for feeding, Levels 4 to 6 pertain to various degrees of oral
women) based on previous studies [31, 32]. food intake and alternative nutrition such as enteral and
Patients who had a disease that was the obvious parenteral nutrition, and Levels 7 to 9 refer to various
cause of the dysphagia were excluded. However, patients degrees of oral intake alone. The reliability and validity of
with stroke, brain injury, neuromuscular disease, head the Food Intake Level Scale have been previously
and neck cancer, or connective tissue disease in whom established [34]. Nutritional status was assessed using
the main cause of dysphagia was considered to be age‐, the Mini Nutritional Assessment‐short form (MNA‐SF)
activity‐, nutrition‐, invasion‐, or cachexia‐related [35‐37]. The MNA‐SF is comprised of six questions
sarcopenia were not excluded. addressing 1) decreased food intake over the past 3
Finally, swallowing muscle strength was assessed months, 2) weight loss over the past 3 months, 3)
by tongue pressure using a maximum tongue pressure mobility, 4) psychological stress or acute disease within
measurement instrument (JMS, Hiroshima, Japan); this is the past 3 months, 5) neuropsychological problems, and
a feasible method in clinical practice, and decreased 6) body mass index.
tongue pressure is thought to be associated with Approximately one‐third of the participants were
sarcopenia and sarcopenic dysphagia [18]. Tongue used to evaluate intra‐rater reliability, and two‐thirds of
pressure measurements using a balloon are becoming the participants were used to evaluate inter‐rater
common in the clinical setting. Tongue pressure reliability. We did not assign the participants to the intra‐
measurements are now covered by medical fees in and inter‐rater reliability evaluations randomly. For inter‐
Japan. Furthermore, several instruments used to rater reliability, patients were assessed twice by a
measure tongue pressure, such as the JMS and Iowa Oral different rater each time. For intra‐rater reliability,
Performance Instrument, are available. Swallowing patients were assessed twice by the same rater, with a 1‐
pressure should be measured primarily to assess the week interval between tests.
strength of the swallowing muscle. Measurement of We analyzed the difference in the MNA‐SF score
swallowing pressure by manometry is available, but it among the no, possible, and probable sarcopenic
requires invasive testing. Therefore, we recommend dysphagia groups. The patients were divided into two
measurement of tongue pressure instead of swallowing groups based on their MNA‐SF score: the no malnutrition
pressure. Indeed, whole‐body sarcopenia affects tongue group (MNA‐SF score: 8‒14) and malnutrition group
pressure [33]. (MNA‐SF score: 0‒7). Statistical analyses were performed
We measured tongue pressure using a balloon using EZR [38] software version 1.31, which was
between the front of the palate and the tongue. developed from the open‐source statistical software R
Measurements were performed once calibration of the (The R Foundation for Statistical Computing, Vienna,
inner‐balloon pressure stabilized to 19.6 kPa. This Austria) [39]. Continuous data were presented as the
calibration was automatically performed by the mean ± standard deviation (SD). Nonparametric data
instrument, and the display screen showed 0.0 kPa if the were expressed as the median and the interquartile
instrument was calibrated successfully. During the range (IQR). Categorical data were described using a
procedure, the patient compresses a balloon attached to percentage. Intra‐class and inter‐class correlation
the tip of the probe between the tongue and front of the coefficients were analyzed using Kappa statistics. The
hard palate with maximum voluntary effort. Tongue difference in the MNA‐SF score between the no


sarcopenic dysphagia and sarcopenic dysphagia groups groups: 32 patients were categorized as having possible
was analyzed by Student’s t‐test and Wilcoxon signed sarcopenic dysphagia and 18 patients were categorized
rank test. The difference in the prevalence rate of as having probable sarcopenic dysphagia. Among all of
sarcopenic dysphagia between the no malnutrition and the patients, 69 had no sarcopenic dysphagia (Figure 2).
malnutrition groups was investigated using the chi‐ The intra‐rater reliability was assessed in 41 patients and
squared test. The risk factors for sarcopenic dysphagia the inter‐rater reliability was assessed in 78 patients. The
were analyzed by logistic regression analysis, using intra‐class coefficient was 0.87 (95% confidence interval
sarcopenic dysphagia as the dependent variable and [CI]: 0.731.01), and the inter‐class coefficient was 0.98
malnutrition, age, and sex as the independent variables. (95% CI: 0.921.02), indicating high intra‐rater and inter‐
rater reliability.
Results Of the 119 total patients, 90 were administered
the MNA‐SF. Analysis of the algorithm’s validity was
A total of 119 patients participated in this study, performed in 67 patients who had no obvious diagnosis
and their characteristics are summarized in Table 2. for dysphagia (Table 3). There were 22 patients in the no
Among the 119 patients, the mean age was 86.1 ± 7.7 sarcopenic dysphagia group and 45 in the sarcopenic
years, and 55 (46%) were men. The majority of the dysphagia (28 and 17 in the possible and probable risk
causative diseases at admission were hip fractures (24) subgroups). The prevalences of sarcopenic dysphagia in
and pneumonia (21). The median of the Food Intake the no malnutrition and malnutrition groups were 45.5%,
Level Scale was 8 (IQR: 710). and 76.0%, respectively. The proportion of patients with
In the diagnostic algorithm used for the sarcopenic dysphagia was significantly higher in the
assessment of sarcopenic dysphagia, 105 patients had malnutrition group than in the no malnutrition group (P =
sarcopenia, 73 of whom had dysphagia with concurrent 0.028). In the logistic regression analysis, malnutrition
sarcopenia. Among the 73 dysphagia patients, 23 were and age were independently associated with sarcopenic
excluded because they had dysphagia caused by another dysphagia (P = 0.013 and 0.003, respectively).
disease. The remaining 50 patients were divided into two


Table 2 Characteristics of patients Figure 2 Distribution of patients according to the risk of sarcopenic dysphagia using the

diagnostic algorithm
Mean ± SD A total of 105 patients had sarcopenia, 73 of whom had dysphagia. There were 32
Characteristics a patients with possible sarcopenic dysphagia, 18 patients with probable sarcopenic

dysphagia, and 69 patients with no sarcopenic dysphagia.
Total number of patients 119
Age, years 86.1 ± 7.7
Male gender, n (%) 55 (46)
2
BMI, kg/m 20.3 ± 4.4
CC, cm 29.2 ± 3.9
Hand grip (right), kg 15.2 ± 7.6
Hand grip (left), kg 14.5 ± 7.2
b
0.42
Gait speed , m/s
(00.9)
c
FILS 8 (710)
d
23.3
MTP , kPa
(15.630.1)
Sarcopenia, n (%) 105 (88)
Dysphagia, n (%) 83 (70)
Diseases causing hospital

admission, n

Hip fracture 24

Pneumonia 21
Aortic aneurysm 6
Cerebral infarction 6
Head and neck cancer 4
Osteoarthritis of the knee 4
Lumbar compression
4
fracture
Spinal cord injury 4
Vertebral fracture 2
ANCA‐associated vasculitis 2
Ileus 2
Malignant lymphoma 2
Rotator cuff tear 2
Lumbar spinal canal stenosis 2
Colorectal cancer 2
Brain tumor 2
Other diseases 30

ANCA, antineutrophil cytoplasmic antibody; BMI, body
mass index; CC, calf circumference; FILS, Food Intake
LEVEL Scale; IQR, interquartile range; MTP, maximum
tongue pressure
a All values are the mean ± standard deviation (SD)
unless otherwise indicated
b Values represent the median (IQR) for n=104
c Values represent the median (IQR)
d Values represent the median (IQR) for n=76


Table 3 Characteristics and univariate analysis for patients assessed by the MNA‐SF

Total Malnutrition No malnutrition
Characteristics P value
(n=67) (n=46) (n=21)
a c
Age, years 82.5 ± 6.7 82.5 ± 6.5 82.5 ± 6.7 0.445
e
Male gender, n (%) 32 (47.8) 22 (47.8) 10 (47.6) 0.934
2 a c
BMI, kg/m 20.4 ± 4.3 19.4 ± 3.67 22.6 ± 4.8 0.007
a c
CC, cm 28.8 ± 4.1 28.0 ± 3.6 30.6 ± 4.6 0.021
a c
Hand grip (right), kg 13.9 ± 6.5 13.3 ± 6.6 15.4 ± 6.2 0.111
a c
Hand grip (left), kg 13.3 ± 6.1 13.1 ± 6.4 13.7 ± 5.4 0.359
a c
Gait speed, m/s 1.32 ± 3.3 0.9 ± 2.5 2.3 ± 4.6 0.127
b d
FILS 8 (6‐9) 8 (4‐9) 8 (7‐10) 0.199
b d
MNA‐SF (score) 7 (4‐8) 5 (4‐7) 9 (8‐10) <0.001
a c
MTP, kPa 22.4 ± 13.4 22.3 ± 14.8 22.6 ± 4.76 0.437
e
Sarcopenia, n (%) 57 (85.1) 40 (87.0) 17 (81.0) 0.713
e
Dysphagia, n (%) 57 (85.1) 42 (91.3) 15 (71.4) 0.060
Sarcopenic dysphagia
e
Probable and Possible, n (%) 45 (67.2) 35 (76.1) 10 (47.6) 0.028
Probable, n (%) 17 (25.3) 14 (30.4) 3 (14.3)
Possible, n (%) 28 (41.8) 21 (45.6) 7 (33.3)
No sarcopenic dysphagia, n (%) 22 (32.8) 11 (23.9) 11 (52.4)

BMI, body mass index; CC, calf circumference; FILS, Food Intake LEVEL Scale; MNA‐SF, Mini Nutritional Assessment Short‐Form; MTP, maximum
tongue pressure
a Mean ± standard deviation
b Median (interquartile range)
c Student`s t test
d Wilcoxon signed rank test
e chi‐squared test

Figure 3 Abridged version of the diagnostic algorithm
Patients with whole‐body sarcopenia, swallowing dysfunction, and no obvious causative disease of dysphagia can be diagnosed with possible
sarcopenic dysphagia without measuring tongue pressure.
a) Cutoff values for hand grip strength (26 kg for men and 18 kg for women) and usual gait speed (0.8 m/s).
2
b) Cutoff values for muscle mass: calf circumference, 34 cm for men and 33 cm for women; general muscle mass (measured by DXA), 7.0 kg/m for
2 2 2
men and 5.4 kg/m for women; general muscle mass (measured by BIA), 7.0 kg/m for men and 5.7 kg/m for women



Discussion In patients with severe cognitive impairment,

measurements of muscle strength and physical function
We performed a cross‐sectional study and made are difficult. Diagnosis of sarcopenic dysphagia in
three important clinical advancements. First, we patients with cognitive impairment is important, because
developed a diagnostic algorithm for sarcopenic cognitive impairment is associated with sarcopenia [43],
dysphagia. Second, we verified the reliability of a and low skeletal muscle mass was associated with poor
diagnostic algorithm for sarcopenic dysphagia by swallowing function in patients with Alzheimer's disease
assessing inter‐ and intra‐rater reliabilities. Third, we [24]. Using the diagnostic algorithm for sarcopenic
verified the validity of the diagnostic algorithm by dysphagia may be difficult in patients with cognitive
evaluating the association between sarcopenic dysphagia impairment. However, measurement of muscle mass and
and malnutrition. assessments of activities of daily living, presence of
We have developed a diagnostic algorithm dysphagia, and obvious conditions considered to be the
specifically to identify sarcopenic dysphagia. The strength main cause of dysphagia are possible. In our personal
of the diagnostic algorithm is that it confers the ability to opinion, cognitively impaired patients with low whole
diagnose probable or possible sarcopenic dysphagia muscle mass, low activities of daily living, swallowing
without assessing swallowing muscle mass. The dysfunction, and no obvious condition considered to be
measurement of swallowing muscle mass is more the main cause of dysphagia can be diagnosed with
difficult to achieve than is the measurement of whole‐ possible sarcopenic dysphagia without assessing muscle
body sarcopenia and tongue pressure. Further, setting a strength or physical functioning. However the reliability
cutoff value for swallowing muscle mass to enable the and validity of this opinion were not verified.
diagnosis of sarcopenic dysphagia is also quite difficult. Therapy for sarcopenic dysphagia includes
Therefore, the improved feasibility of diagnosing rehabilitation for the dysphagia and treatment for the
sarcopenic dysphagia using the diagnostic algorithm can sarcopenia [1], both of which require a multidisciplinary
promote its research and management in clinical medical team. Regardless of whether there is a possible
practice. or probable risk of sarcopenic dysphagia, it is essential to
We verified the reliability of the diagnostic treat sarcopenic dysphagia using a combination of
algorithm for sarcopenic dysphagia. The kappa nutritional management to increase muscle mass and
coefficients for the intra‐ and inter‐class reliabilities were early dysphagia rehabilitation [1, 2]. Resistance training
0.87 and 0.98, respectively, indicating that this diagnostic for the swallowing muscles, such as head‐raising
algorithm is highly reliable; therefore, all qualified exercises and tongue‐strengthening exercises, should be
medical staff will be able to utilize this tool. included in dysphagia rehabilitation, especially in cases of
We also verified the validity of the diagnostic probable sarcopenic dysphagia. Early oral intake has
algorithm for sarcopenic dysphagia. Malnutrition was been shown to promote an early hospital discharge in
independently associated with sarcopenic dysphagia. older patients with pneumonia [44, 45]. Furthermore,
Malnutrition is an independent risk factor for sarcopenic early physical therapy decreases in‐hospital mortality
dysphagia in hospitalized older patients [40]. after aspiration pneumonia [46]. The improvement of
Furthermore, nutrition improvement seems to be nutrition and early dysphagia rehabilitation may prevent
necessary for patients with sarcopenic dysphagia to and treat sarcopenic dysphagia, by improving activity‐
improve swallowing function [7, 41, 42]. Therefore, an and nutrition‐related sarcopenia.
association between malnutrition and sarcopenic This study has some limitations. First, the sample
dysphagia is reasonable. size of the study was small, and we did not include
Not every examiner has an instrument to measure healthy older individuals. While investigations of healthy
tongue pressure. When tongue pressure measurements older individuals would be useful, diagnosis and
are not available, we suggest two alternatives. First, we treatment of sarcopenic dysphagia in hospitalized
propose using an abridged version of the diagnostic patients are clinically urgent. Second, selection bias
algorithm for cases in which tongue pressure possibly exists because consecutive sampling was not
measurement is difficult. Patients with whole‐body used in this study. Therefore, the proportion of general
sarcopenia, swallowing dysfunction, and no obvious sarcopenia among all patients may be not typical. Third,
causative disease of dysphagia can be diagnosed with we used calf circumference for general muscle mass
possible sarcopenic dysphagia without measuring tongue measurements, with cutoff values of <34 cm for men and
pressure (Figure 3). Second, we suggest assessing head <33 cm for women. DXA or BIA are more appropriate
lifting strength, which does not require any instruments. tools for measuring muscle mass, and a different cutoff
The ability to lift the head reflects the strength of the value for calf circumference (<33 cm for men) has been
suprahyoid muscles, and individuals who cannot lift their reported previously [47, 48]. Finally, the investigation of
head in the supine position tend to have dysphagia [19]. validity was performed in only 67 patients, because no
However, we recommend tongue pressure MNA‐SF data were available in the remaining patients.
measurements to assess the strength of the swallowing In conclusion, we have developed and verified the
muscle. reliability and validity of a diagnostic algorithm for
sarcopenic dysphagia. All older patients with sarcopenia

or dysphagia should be assessed for sarcopenic supported by a research Grant‐in‐Aid for Scientific
dysphagia to see if it also exists, as it can occur and Research C (no. 16K01460) from the Ministry of
requires treatment that involves not only dysphagia Education, Science, Culture, Sports, Science, and
rehabilitation but also nutritional improvement. Technology of Japan. Hidetaka Wakabayashi received
reimbursement for travel expenses from Nestlé Health
Acknowledgment Sciences. Takashi Mori, Ichiro Fujishima, Fumiko Oshima,
Masataka Itoda, Kenjiro Kunieda, Jun Kayashita, Shinta
The authors certify that they comply with the Nishioka, Akiko Sonoda, Yoshitosi Kuroda, Minoru
ethical guidelines for authorship and publishing of the Yamada, Sumito Ogawa declare no conflicts of interest.
Journal of Cachexia, Sarcopenia and Muscle ‐ Clinical The study protocol was approved by the ethics
Reports (von Haehling S, Ebner N, Morley JE, Coats AJS, committee of Hamamatsu City Rehabilitation Hospital.
Anker SD. Ethical guidelines for authorship and This study has been performed in accordance with the
publishing in the Journal of Cachexia, Sarcopenia and ethical standards established in the 1964 Declaration of
Muscle ‐ Clinical Reports. J Cachexia Sarcopenia Muscle Helsinki and later amendments.
Clinical Reports 2016;1;e28:1‐2). This work was

References

1. Wakabayashi H. Presbyphagia and 8. Cruz‐Jentoft AJ, Landi F, Schneider geniohyoid muscle atrophy is
sarcopenic dysphagia: association SM, Zúñiga C, Arai H, Boirie Y, Chen related to aspiration status in
between aging, sarcopenia, and LK, Fielding RA, Martin FC, Michel JP, healthy older adults. J Gerontol A
deglutition disorders. J Frailty Aging Sieber C, Stout JR, Studenski SA, Biol Sci Med Sci. 2013;68:853‐60.
2014;3:97‐103. Vellas B, Woo J, Zamboni M, 15. Molfenter SM, Amin MR, Branski RC,
2. Wakabayashi H, Sakuma K. Cederholm T. Prevalence of and Brumm JD, Hagiwara M, Roof SA,
Rehabilitation nutrition for interventions for sarcopenia in Lazarus CL. Age‐related changes in
sarcopenia with disability: a ageing adults: a systematic review. pharyngeal lumen size: a
combination of both rehabilitation Report of the International retrospective MRI analysis.
and nutrition care management. J Sarcopenia Initiative (EWGSOP and Dysphagia. 2015;30:321‐27.
Cachexia Sarcopenia Muscle IWGS). Age Ageing 2014;43:748‐59. 16. Yoshida M, Kikutani T, Tsuga K,
2014;5:269‐77. 9. Carrión S, Roca M, Costa A, Arreola Utanohara Y, Hayashi R, Akagawa Y.
3. Clavé P, Shaker R. Dysphagia: V, Ortega O, Palomera E, Serra‐Prat Decreased tongue pressure reflects
current reality and scope of the M, Cabré M, Clavé P. Nutritional symptom of dysphagia. Dysphagia.
problem. Nat Rev Gastroenterol status of older patients with 2006;21:61‐65.
Hepatol 2015;12:259‐70. oropharyngeal dysphagia in a 17. Konaka K, Kondo J, Hirota N, Tamine
4. Cruz‐Jentoft AJ, Baeyens JP, Bauer chronic versus an acute clinical K, Hori K, Ono T, Maeda Y, Sakoda S,
JM, Boirie Y, Cederholm T, Landi F, situation. Clin Nutr. 2016. doi: Naritomi H. Relationship between
Martin FC, Michel JP, Rolland Y, 10.1016/j.clnu.2016.07.009. tongue pressure and dysphagia in
Schneider SM, Topinková E, 10. Chen LK, Lee WJ, Peng LN, Liu LK, stroke patients. Eur Neurol.
Vandewoude M, Zamboni M; Arai H, Akishita M, Asian Working 2010;64:101‐7.
European Working Group on Group for Sarcopenia. Recent 18. Maeda K, Akagi J. Decreased tongue
Sarcopenia in Older People. advances in sarcopenia research in pressure is associated with
Sarcopenia: European consensus on Asia: 2016 update from the Asian sarcopenia and sarcopenic
definition and diagnosis: Report of Working Group for Sarcopenia. J Am dysphagia in the elderly. Dysphagia.
the European Working Group on Med Dir Assoc. 2016;17:767.e1‐7. 2015;30:80‐87.
Sarcopenia in Older People. Age 11. Yatera K, Naito K, Noguchi S, Akata 19. Wakabayashi H, Sashika H,
Ageing 2010;39:412‐23. K, Yamasaki K, Nishida C, Kawanami Matsushima M. Head lifting strength
5. Maeda K, Akagi J. Sarcopenia is an T, Sakamoto N, Kido T, Ishimoto H, is associated with dysphagia and
independent risk factor of dysphagia Mukae H. Clinical efficacy and safety malnutrition in frail older adults.
in hospitalized older people. Geriatr of high‐dose doripenem in Japanese Geriatr Gerontol Int. 2015;15:410‐
Gerontol Int. 2016;16:515‐21. patients with pneumonia. J Infect 16.
6. Chen LK, Liu LK, Woo J, Assantachai Chemother. 2016;22:137‐42. 20. Kuroda Y, Kuroda R. Relationship
P, Auyeung TW, Bahyah KS, Chou 12. Saitoh M, Ishida J, Konishi M, between thinness and swallowing
MY, Chen LY, Hsu PS, Krairit O, Lee Springer J. The concept that focuses function in Japanese older adults:
JS, Lee WJ, Lee Y, Liang CK, on oral motor and feeding function implications for sarcopenic
Limpawattana P, Lin CS, Peng LN, in cancer patients with muscle dysphagia. J Am Geriatr Soc.
Satake S, Suzuki T, Won CW, Wu CH, wasting: Skeletal muscle mass is 2012;60:1785‐86.
Wu SN, Zhang T, Zeng P, Akishita M, associated with severe dysphagia in 21. Kuroda Y. Relationship between
Arai H. Sarcopenia in Asia: cancer patients. J Cachexia swallowing function, and functional
consensus report of the Asian Sarcopenia Muscle 2016;7:233‐34. and nutritional status in hospitalized
Working Group for Sarcopenia. J Am 13. Tamura F, Kikutani T, Tohara T, elderly individuals. Int J Speech Lang
Med Dir Assoc 2014;15:95‐101. Yoshida M, Yaegaki K. Tongue Pathol Audiol. 2014;2:20‐26.
7. Wakabayashi H, Uwano R. thickness relates to nutritional 22. Wakabayashi H, Matsushima M,
Rehabilitation nutrition for possible status in the elderly. Dysphagia. Uwano R, Watanabe N, Oritsu H,
sarcopenic dysphagia after lung 2012;27:556‐61. Shimizu Y. Skeletal muscle mass is
cancer surgery: a case report. Am J 14. Feng X, Todd T, Lintzenich CR, Ding J, associated with severe dysphagia in
Phys Med Rehabil 2016;95:e84‐9. Carr JJ, Ge Y, Browne JD, Kritchevsky cancer patients. J Cachexia
SB, Butler SG. Aging‐related Sarcopenia Muscle. 2015;6:351‐57.


23. Sagawa K, Kikutani T, Tamura F, 32. Barbosa‐Silva TG, Bielemann RM, Rehabilitation and Nutritional

Yoshida M. Factors related to Gonzalez MC, Menezes AMB. Support: A Comprehensive
skeletal muscle mass in the frail Prevalence of sarcopenia among Approach. J Acad Nutr Diet.
elderly. Odontology. 2017;105:91‐95 community‐dwelling elderly of a 2016;116:573‐77
24. Takagi D, Hirano H, Watanabe Y, medium‐sized South American city: 43. Maeda K, Akagi J. Cognitive
Edahiro A, Ohara Y, Yoshida H, Kim results of the COMO VAI? Study. J impairment is independently
H, Murakami K, Hironaka S. Cachexia Sarcopenia Muscle. associated with definitive and
Relationship between skeletal 2016;7:136‐43 possible sarcopenia in hospitalized
muscle mass and swallowing 33. Machida N, Tohara H, Hara K, older adults: The prevalence and
function in patients with Alzheimer's Kumakura A, Wakasugi Y, Nakane A, impact of comorbidities. Geriatr
disease. Geriatr Gerontol Int. Minakuchi S. Effects of aging and Gerontol Int. 2016. doi:
2017;17:402‐9. sarcopenia on tongue pressure and 10.1111/ggi.12825.
25. Butler SG, Stuart A, Leng X, Wilhelm jaw‐opening force. Geriatr Gerontol 44. Koyama T, Maeda K, Anzai H,
E, Rees C, Williamson J, Kritchevsky Int. 2017;17:295‐301. Koganei Y, Shamoto H, Wakabayashi
SB. The relationship of aspiration 34. Kunieda K, Ohno T, Fujishima I, Hojo H. Early commencement of oral
status with tongue and handgrip K, Morita T. Reliability and validity of intake and physical function are
strength in healthy older adults. J a tool to measure the severity of associated with early hospital
Gerontol A Biol Sci Med Sci. dysphagia: the Food Intake LEVEL discharge with oral intake in
2011;66:452‐58. Scale. J Pain Symptom Manage. hospitalized elderly individuals with
26. Hathaway B, Baumann B, Byers S, 2013;46:201‐6. pneumonia. J Am Geriatr Soc.
Wasserman‐Wincko T, Badhwar V, 35. Vellas B, Villars H, Abellan G, Soto 2015;63:2183‐85.
Johnson J. Handgrip strength and ME, Rolland Y, Guigoz Y, Morley JE, 45. Maeda K, Koga T, Akagi J. Tentative
dysphagia assessment following Chumlea W, Salva A, Rubenstein LZ, nil per os leads to poor outcomes in
cardiac surgery. Laryngoscope. Garry P. Overview of the MNA® ‐ its older adults with aspiration
2015;125:2330‐32. history and challenges. J Nutr Health pneumonia. Clin Nutr.
27. Murakami M, Hirano H, Watanabe Y, Aging 2006;10:456‐65. 2016;35:1147‐52.
Sakai K, Kim H, Katakura A. 36. Rubenstein LZ, Harker JO, Salva A, 46. Momosaki R, Yasunaga H, Matsui H,
Relationship between chewing Guigoz Y, Vellas B. Screening for Horiguchi H, Fushimi K, Abo M.
ability and sarcopenia in Japanese undernutrition in geriatric practice: Effect of early rehabilitation by
community‐dwelling older adults. developing the Short‐Form Mini physical therapists on in‐hospital
Geriatr Gerontol Int. 2015;15:1007‐ Nutritional Assessment (MNA‐SF). J mortality after aspiration
12 Geront 2001;56A:M366‐72. pneumonia in the elderly. Arch Phys
28. Shiozu H, Higashijima M, Koga T. 37. Guigoz Y. The Mini‐Nutritional Med Rehabil 2015;96:205‐9.
Association of sarcopenia with Assessment (MNA®) review of the 47. Bahat G, Tufan A, Tufan F, Kilic C,
swallowing problems, related to literature ‐ what does it tell us? J Akpinar TS, Kose M, Erten N, Karan
nutrition and activities of daily living Nutr Health Aging 2006;10:466‐87. MA, Cruz‐Jentoft AJ. Cut‐off points
of elderly individuals. J Phys Ther 38. Kanda Y. Investigation of the freely to identify sarcopenia according to
Sci. 2015;27:393‐96. available easy‐to‐use software ‘EZR’ European Working Group on
29. Nishioka S, Okamoto T, Takayama for medical statistics. Bone Marrow Sarcopenia in Older People
M, Urushihara M, Watanabe M, Transplantation. 2013;48:452‐8. (EWGSOP) definition. Clin Nutr.
Kiriya Y, Shintani K, Nakagomi H, 39. Institute for Statistics and 2016 ;35:1557‐63.
Kageyama N. Malnutrition risk Mathematics of 48. Kaiser M, Bauer J, Ramsch C, Uter
predicts recovery of full oral intake Wirtschaftsuniversität Wien. The W, Guigoz Y, Cederholm T, Thomas
among older adult stroke patients Comprehensive R Archive Network. DR, Anthony P, Charlton KE, Maggio
undergoing enteral nutrition: 2016. http://cran.r‐project.org/ M, Tsai AC, Grathwohl D, Vellas B,
Secondary analysis of a multicentre Accessed 22 August 2016. Sieber CC; MNA‐International
survey (the APPLE study). Clin Nutr. 40. Maeda K, Takaki M, Akagi J. Group. Validation of the mini
2016. doi: Decreased Skeletal Muscle Mass and nutritional assessment short‐form
10.1016/j.clnu.2016.06.028. Risk Factors of Sarcopenic (MNA®‐SF); a practical tool for
30. Maeda K, Akagi J. Treatment of Dysphagia: A Prospective identification of nutritional status. J
sarcopenic dysphagia with Observational Cohort Study. J Nutr Heal Aging 2009;13:782‐88.
rehabilitation and nutritional Gerontol A Biol Sci Med Sci. 2016. 49. von Haehling S, Ebner N, Morley JE,
support: a comprehensive approach. doi: 10.1093/gerona/glw190. Coats AJ, Anker SD. Ethical
J Acad Nutr Diet 2016;116:573‐77. 41. Hashida N, Shamoto H, Maeda K, guidelines for authorship and
31. Kawakami R, Murakami H, Sanada K, Wakabayashi H, Suzuki M, Fujii T. publishing in the Journal of
Tanaka N, Sawada SS, Tabata I, Rehabilitation and nutritional Cachexia, Sarcopenia and Muscle
Higuchi M, Miyachi M. Calf support for sarcopenic dysphagia Clinical Report. J Cachexia
circumference as a surrogate marker and tongue atrophy after Sarcopenia Muscle Clinical Reports
of muscle mass for diagnosing glossectomy: A case report. 2016;1;e1:1‐2.
sarcopenia in Japanese men and Nutrition. 2017;35:128‐31.
women. Geriatr Gerontol Int. 42. Maeda K, Akagi J. Treatment of
2015;15:969‐76. Sarcopenic Dysphagia with


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Introduction [11] following cancers and heart diseases. Moreover,

Table 2 Characteristics of patients Figure 2 Distribution of patients according to the risk of sarcopenic dysphagia using the

Probable, n (%) 17 (25.3) 14 (30.4) 3 (14.3)

Possible, n (%) 28 (41.8) 21 (45.6) 7 (33.3)

No sarcopenic dysphagia, n (%) 22 (32.8) 11 (23.9) 11 (52.4)

Discussion In patients with severe cognitive impairment,

23. Sagawa K, Kikutani T, Tamura F, 32. Barbosa‐Silva TG, Bielemann RM, Rehabilitation and Nutritional

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