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DOI: 10.1111/ggi.

13627

ORIGINAL ARTICLE

EPIDEMIOLOGY, CLINICAL PRACTICE AND HEALTH

Association between sarcopenia and sleep disorder in older


patients with diabetes
Satoshi Ida,1 Ryutaro Kaneko,1 Hiroaki Nagata,2 Yoshinori Noguchi,2 Yasuha Araki,2 Mari Nakai,3
Sho Ito,3 Yuki Ishihara,1 Kanako Imataka1 and Kazuya Murata1
1 Aim: In the present study, we aimed to examine the association between sarcopenia and
Department of Diabetes and
Metabolism, Ise Red Cross sleep disorder in older patients with diabetes using the Japanese version of SARC-F (SARC-
F-J).
Hospital, Ise-shi, Japan
2
Department of Pharmacy, Ise Red Methods: Outpatients with diabetes (aged ≥65 years) at the Ise Red Cross Hospital were
Cross Hospital, Ise-shi, Japan included in the present study. We used the Japanese version of the Pittsburgh Sleep Quality
3
Department of Clinical Index, which is a self-administered questionnaire, to measure sleep disorder. To evaluate sar-
copenia, we used SARC-F-J, a self-administered questionnaire, comprising five items. For
Psychology Team, Ise Red Cross
multiple logistic regression analysis, the dependent variable was sleep disorder and the explan-
Hospital, Ise-shi, Japan
atory variable was sarcopenia, and these were used for calculating the odds ratios of sarcope-
nia with regard to sleep disorder.
Correspondence
Results: In total, 318 patients were included in this study (189 men and 129 women). The
Dr Satoshi Ida MD, MPH,
prevalence of sarcopenia was 22.5% and that of sleep disorder was 44.8%. Adjusted odds
Department of Diabetes and
ratios of sarcopenia and sleep disorder were 6.04 in men (95% CI 1.71–21.36, P = 0.005) and
Metabolism, Ise Red Cross 6.33 in women (95% CI 1.91–20.97, P = 0.003).
Hospital, 1-471-2, Funae,
Conclusions: We found a statistically significant association between sarcopenia and sleep
1-chome, Ise-shi, Mie 516-8512,
disorder in older patients with diabetes using SARC-F-J. Therefore, older patients with diabe-
Japan.
tes should be cautioned regarding sleep disorder if they are diagnosed with sarcopenia. Ger-
Email: bboy98762006@yahoo.co.jp iatr Gerontol Int 2019; ••: ••–••.

Received: 25 May 2018 Keywords: confidence interval, diabetes, elderly patients, sarcopenia, sleep disorder.
Revised: 12 December 2018
Accepted: 10 January 2019

Introduction disorder.3,11,12 However, to the best of our knowledge, there is no


study on the association between sarcopenia and sleep disorders
Sleep disorder refers to all diseases in which abnormal sleep leads in older patients with diabetes using SARC-F-J. Therefore, we
to various social dysfunctions and a decline in the quality of life, aimed to evaluate this association in older patients with diabetes
and it is considered to be a serious health problem.1 The prevalence using SARC-F-J and carry out cross-sectional examinations.
of sleep disorder in patients with diabetes is 37–50%,2 which is
higher than that in the general population,3 and it increases with Methods
age.1 Thus, the prevalence of sleep disorder in older patients with
diabetes is possibly even higher. The association of sleep disorder Study design and patients
with a decline in activities of daily living, cognitive function, falls and
The present cross-sectional study targeted outpatients with diabe-
cardiovascular death has been clearly shown.4,5 Therefore, sleep dis-
tes at the Ise Red Cross Hospital located in Ise City, Mie Prefec-
order in older patients with diabetes is a serious health problem.
ture, Japan. This study was approved by the ethics committee of
In aging societies, sarcopenia, which is characterized by a
the Ise Red Cross Hospital, and written informed consent was
decline in the muscle mass, muscle strength and physical func-
obtained from all participants. Eligibility criteria were having dia-
tions, is considered to be a serious problem, and its association
betes, being an outpatient between June and November 2017, and
with declined activities of daily living, quality of life and death has
age ≥65 years. The exclusion criteria were patients with a history
been established.6 Patients with diabetes have a higher prevalence
of secondary diabetes, alcoholism, severe mental illness, malignant
of sarcopenia than those without diabetes.7 Thus, it is important
tumor, pacemaker use, bilateral knee replacement surgery, hip
to caution patients with diabetes if they are diagnosed with sarco-
replacement, home oxygen therapy, those with a diagnosis of
penia. However, the diagnosis of sarcopenia is complex and diffi-
heart failure within 6 months and those unable to participate in
cult to identify during routine examination. Malmstrom et al.
the survey by themselves.10
developed SARC-F, a simple screening tool for sarcopenia, and
verified its validity.8,9 In recent years, we developed the Japanese
Measurement of sleep disorder
version of SARC-F (SARC-F-J) for older patients with diabetes.10
Its sensitivity was 14.6% in men and 33.3% in women, and its We used the Japanese version of the Pittsburgh Sleep Quality
specificity was 85.8% and 72.4%, respectively, when using the Index (PSQI-J) for measuring sleep disorder.13 PSQI-J is a self-
definition of sarcopenia by the European Working Group on Sar- administered questionnaire widely used for evaluating sleep disor-
copenia in Older People as a reference.6 der; it includes seven components (subjective sleep quality, sleep
A study that targeted older individuals living in an area latency, sleep duration, habitual sleep efficiency, sleep distur-
reported an association between sarcopenia and sleep bances, use of sleeping medication and daytime dysfunction) that

© 2019 Japan Geriatrics Society | 1


S Ida et al.

are scored between 0 and 3 points; that is, a total score of 0–50, and lower scores indicate a lower cognitive function. Sensi-
0–21 points. A higher score indicates worse quality of sleep. This tivity of the Japanese version of Test Your Memory, when defining
scale is highly reliable and valid, and provides qualitative and the cognitive function decline at ≤44 points, was 76% and speci-
quantitative information on sleep, which could be compared ficity was 74%.18 In the present study, we diagnosed cognitive
between individuals and groups. In the present study, a total score function decline at a Japanese version of Test Your Memory score
of ≥5.5 was considered to be an indicator of sleep disorder, based of ≤44 points. In terms of living alone, we used a dichotomous
on the results of a previous study.13 question where patients were asked to answer “yes” or “no” to the
question, “Do you live alone right now?”

Evaluation of sarcopenia using SARC-F-J


Statistical analysis
To evaluate sarcopenia, we used SARC-F-J, a self-administered
questionnaire, comprising five items (strength, assistance in walk- Patient backgrounds were classified by diagnosis of sarcopenia
ing, rise from a chair, climb stairs and falls).10 Responses were based on SARC-F-J and by sex. Continuous variables were com-
provided at three levels of “no problem at all” (0 points), “some pared between groups using the t-test, whereas binary variables
problems” (1 point) and “very problematic or not possible” were compared between the groups using the χ2-test. With sleep
(2 points); however, responses to questions on falls were given in disorder as the dependent variable and sarcopenia as the explana-
three levels: never, one to three times and four or more times. tory variable, we calculated the adjusted odds ratio for sarcopenia
The maximum score is 10 points (range 0–10), with a score of with regard to sleep disorder using the logistic regression analysis.
≥4 points indicating the presence of sarcopenia. On clinical diagnosis, variables to be adjusted were age, BMI,
HbA1c level, smoking, alcohol consumption, number of comor-
bidities (hypertension, dyslipidemia, diabetic retinopathy, diabetic
Measurement of other variables
neuropathy, diabetic nephropathy and cardiovascular disease),
We also noted age, sex, body mass index (BMI; weight [kg] / height depression, cognitive impairment and living alone, according to
squared [m2]), smoking, alcohol consumption, type of diabetes previous studies.3,12 The significance level (two-tailed) was <0.05,
(type 1, type 2 or other), duration of diabetes, hemoglobin A1c and we used Stata version 12.0 (StataCorp, College Station, TX,
(HbA1c) level, hypertension, dyslipidemia, insulin resistance, dia- USA) for the analysis.
betic retinopathy, diabetic neuropathy, diabetic nephropathy, car-
diovascular disease, use of oral hypoglycemic agents, depression, Results
cognitive impairment and living alone. Classification of the type of
diabetes (type 1, type 2 or other) was based on the classification
A total of 352 participants who met the eligibility criteria were
by the Japan Diabetes Society.14 The serum lipid level was mea-
included in the study. A total of 34 patients with missing data were
sured using the enzyme method, and the plasma glucose level was
excluded, and the remaining 318 (189 men and 129 women)
measured using the glucose oxidase method. For HbA1c level, we
patients were used as the analysis set. The prevalence of sarcope-
used high-pressure liquid chromatography and noted results using
nia was 22.5% (19.0% in men and 27.1% in women). The preva-
the National Glycohemoglobin Standardization Program (www.
lence of sleep disorder was 44.8% (44.4% in men and 44.9% in
ngsp.org). Systolic and diastolic blood pressures were measured in
women).
the examination room, and any of the following was considered to
Table 1 shows patient backgrounds. Men in the sarcopenic
indicate hypertension: systolic blood pressure of ≥130 mmHg, dia-
group had a higher prevalence of hypertension and cognitive
stolic blood pressure of ≥80 mmHg or use of an antihypertensive
impairment, and women in the sarcopenic group were older and
drug. In terms of lipids, any of the following was considered to
had longer duration of diabetes than those in the non-sarcopenic
indicate dyslipidemia: triglycerides of ≥150 mg/dL, high-density
group. The prevalence of diabetic neuropathy, cardiovascular dis-
lipoprotein cholesterol level of <40 mg/dL, low-density lipoprotein
ease and depression was higher among women than among men
cholesterol level of ≥120 mg/dL (or low-density lipoprotein cho-
in the sarcopenic group. Men and women in the sarcopenic group
lesterol of ≥100 mg/dL if there was coronary artery disease) or use
had a higher prevalence of sleep disorder than those in the non-
of a lipid-lowering drug. The insulin resistance index was calcu-
sarcopenic group.
lated as triglycerides / high-density lipoprotein cholesterol.15 Dia-
The results of the logistic regression analysis are shown in
betic retinopathy was diagnosed by an ophthalmologist. Diabetic
Table 2. The adjusted odds ratio of sarcopenia and sleep disorder
neuropathy was determined by a decline in Achilles tendon reflex,
was 6.04 (95% CI 1.71–21.36; P = 0.005) in men and 6.33 (95%
hypesthesia in the lateral malleolus and/or nerve conduction test
CI 1.91–20.97; P = 0.003) in women. In men and women, there
abnormality. The presence of cardiovascular disease was deter-
was a statistically significant association between sarcopenia and
mined by current or past history of ischemic heart diseases, such
sleep disorder.
as angina pectoris and myocardial infarction, or cerebrovascular
diseases, such as cerebral infraction. To measure depression, we
used the Japanese version of the Patient Health Questionnaire 9 Discussion
that was developed and validated by Muramatsu et al.16 Symptoms
of the previous 2 weeks were evaluated on a 4-point scale (almost In the present study of older patients with diabetes, we exam-
every day, 3 points; more than half of the time, 2 points; several ined the association between sarcopenia and sleep disorder
days, 1 point; and never, 0 points) with a total score of 0–27, and using SARC-F-J. The results showed that in men and women,
higher scores indicating more severe depression. In the present sarcopenia has a statistically significant association with sleep
study, we diagnosed depression at ≥5 points on the Japanese ver- disorders.
sion of the Patient Health Questionnaire 9, based on the results of The ratio of patients with sleep disorder in the present study
a previous study.17 To measure cognitive function, we used the was 44.8% (men, 44.4%; women, 44.9%). The following are con-
Japanese version of Test Your Memory, which is a self- sidered to be possible underlying mechanisms of developing sleep
administered cognitive function evaluation tool developed by disorder because of diabetes. Diabetic neuropathy as a result of
Hanyu et al., and its validity has been verified.18 It includes chronic hyperglycemia, overactivity of the sympathetic nervous
10 points for orientation, 2 points for sentence copying, 3 points system, microarousals caused by chronic hyperglycemia or noc-
for knowledge, 4 points for calculation, 4 points for language flu- turnal hypoglycemia might cause sleep disorders.19 It is also possi-
ency, 4 points for similarities, 5 points for naming items, 7 points ble that sleep apnea, which is commonly observed in patients with
for two visual space/composition problems, 6 points for recollec- diabetes, is associated with sleep disorders.20 Furthermore,
tion of a sentence and 5 points for help; that is, total scores of patients with diabetes often have comorbidities and complications,

2 | © 2019 Japan Geriatrics Society


Sarcopenia with sleep disorder

Table 1 Patient backgrounds

Men Women
No sarcopenia Sarcopenia P No sarcopenia Sarcopenia P
n = 153 n = 36 n = 94 n = 35
(80.9%) (19.1%) (72.8%) (27.2%)
Mean age, years (SD) 70.9 (5.5) 72.7 (6.3) 0.083 71.3 (5.5) 74.2 (6.8) 0.014*
Mean BMI, kg/m2 (SD) 24.0 (4.3) 24.6 (4.3) 0.451 23.6 (4.4) 24.2 (4.6) 0.109
T1DM/T2DM/other (%) 5.9/92.1/2.0 3.0/97.0/0 0.566 9.6/89.3/1.1 9.7/87.1/3.2 0.707
Mean HbA1c, % (SD) 7.3 (1.2) 7.0 (0.9) 0.196 7.4 (0.9) 7.6 (1.4) 0.269
Mean duration of diabetes, years (SD) 17.9 (11.3) 20.4 (11.4) 0.255 16.1 (10.4) 20.6 (10.5) 0.042*
Alcohol consumption (%) 30.4 29.6 0.931 8.7 8.5 0.969
Smoking (%) 35.1 37.0 0.849 2.1 2.8 0.807
Hypertension (%) 79.4 94.1 0.044* 72.3 77.4 0.578
Dyslipidemia (%) 71.7 64.7 0.418 72.8 83.3 0.246
Mean TG/HDL-C ratio (SD) 2.9 (2.1) 6.3 (15.8) 0.017* 2.4 (1.6) 3.1 (2.1) 0.055
Retinopathy (%) 34.3 41.3 0.477 40.2 44.8 0.663
Neuropathy (%) 59.4 72.2 0.157 54.2 77.1 0.008*
Nephropathy (%) 54.5 76.4 0.063 48.8 53.3 0.672
Cardiovascular diseases (%) 24.4 38.2 0.104 8.6 36.6 <0.001*
Depression (%) 58.8 72.2 0.137 54.2 77.1 0.018*
Cognitive impairment (%) 13.0 30.5 0.011* 21.2 31.4 0.230
Living alone (%) 14.7 11.4 0.610 19.7 18.1 0.247
Oral hypoglycemic agents (%) 80.2 70.5 0.215 78.7 70.9 0.375
GLP-1 analog (%) 9.8 9.0 0.891 14.8 9.6 0.463
Insulin (%) 64.4 75.7 0.213 59.5 74.1 0.143
Mean PSQI scores (SD) 5.2 (3.4) 6.7 (3.8) 0.025* 4.9 (3.1) 7.1 (3.7) <0.001*
Sleep disorder (%) 40.5 61.1 0.025* 36.1 68.5 <0.001*
*P < 0.05. Cardiovascular diseases are defined as angina pectoris, myocardial infarction and stroke. BMI, body mass index; GLP-1, glucagon-like
peptide-1; HbA1c, hemoglobin A1c; HDLC, high-density lipoprotein cholesterol; SD, standard deviation; T1DM/T2DM, type 1/type 2 diabetes
mellitus; TG, triglycerides; PSQI, Pittsburgh Sleep Quality Index.

Table 2 Factors associated with odds ratios of sleep disorder using a logistic regression analysis

Male Female
Adjusted OR P Adjusted OR P
(95% CI) (95% CI)
Age (per year increase) 0.90 (0.83–0.98) 0.022* 0.94 (0.87–1.02) 0.196
BMI (per 1 kg/m2 increase) 1.00 (0.88–1.13) 0.936 1.00 (0.90–1.11) 0.997
HbA1c level (per 1% increase) 0.60 (0.38–0.96) 0.036* 0.73 (0.48–1.11) 0.153
Alcohol consumption (vs no) 0.51 (0.18–1.43) 0.204 0.95 (0.22–4.11) 0.955
Smoking (vs no) 0.39 (0.15–1.04) 0.060 0.92 (0.04–19.15) 0.959
Depression (vs no) 0.87 (0.33–2.24) 0.780 0.52 (0.19–1.38) 0.193
Living alone (vs no) 1.71 (0.54–5.38) 0.780 1.41 (0.45–4.38) 0.548
No. comorbidities (per 1 increase) 0.72 (0.51–1.02) 0.070 1.35 (0.98–1.85) 0.064
Cognitive impairment (vs no) 2.68 (0.71–10.12) 0.145 0.62 (0.19–1.97) 0.419
Sarcopenia (vs no) 6.04 (1.71–21.36) 0.005* 6.33 (1.91–20.97) 0.003*
*P < 0.05. Comorbidities include chronic condition, including hypertension, dyslipidemia, retinopathy, neuropathy, nephropathy and cardiovascu-
lar diseases (angina pectoris, myocardial infarction and stroke). BMI, body mass index; CI, confidence interval; HbA1c, hemoglobin A1c; OR, odds
ratio.

and the mental burden of treatment in addition to the disease those of patients in the previous study could have been another
itself might cause sleep disorders.21 In the present study, we did reason for the different PSQI scores in the present study.
not evaluate the sympathetic nervous system, frequency of hypo- The prevalence of sarcopenia using SARC-F-J in the present
glycemia and sleep apnea; therefore, we cannot comment on the study was 22.5% (men, 19.0%; women, 27.1%). In a previous
involvement of these factors. However, the frequency of complica- study, the prevalence of sarcopenia in older patients with diabetes
tions is high, and this might have been involved with sleep disor- was 19% in men and 27% in women, which is similar to that
der. The PSQI score of older patients with diabetes with observed in the present study.7 In another study that targeted dia-
complications has been reported to be 7.7,22 and in the present betes patients, the prevalence of sarcopenia was 17.6%.24 Presum-
study, the PSQI score was slightly lower in the sarcopenic group. ably, differences in participant age, comorbidities and sarcopenia
A previous study had a larger number of women, and the preva- definition strongly influenced the outcomes. Compared with
lence of cardiovascular disease was high. The fact that participants patients without diabetes, those with diabetes had a higher preva-
were women or had a high prevalence of concomitant diseases lence of sarcopenia.7 The mechanisms underlying this might be
can be considered to be associated with sleep disorder,23 and protein hypermetabolism, oxidative stress and inflammatory cyto-
could have been the reason why PSQI scores in the present study kines.25 Diagnosis of sarcopenia is complex and difficult during
were lower than those reported in the previous study. Further- routine examination. Thus, here we used SARC-F-J, a simple
more, the fact that the age and race of patients were different from screening tool for sarcopenia that we recently developed, for

© 2019 Japan Geriatrics Society | 3


S Ida et al.

evaluating sarcopenia. However, the sensitivity of SARC-F-J used validity of sarcopenia or sleep disorder prevalence because of the
for evaluating sarcopenia was low;10 thus, the prevalence of sarco- use of only SARC-F-J and PSQI-J evaluations, interpretation of
penia in the present study might be underestimated. Therefore, the results requires caution. Second, adjustments for confounding
interpretation should be made with caution. factors might be insufficient. It is possible that factors, such as
Patient background regarding sarcopenia in the present study physical activities and nutritional conditions, that were not evalu-
showed that among women, there were more complications of ated and adjusted for in the present study might have impacted
diabetes and depression in the sarcopenic group compared with the results. Third, we grouped type 1 and type 2 diabetes patients
those in the non-sarcopenic group. This is perhaps because together in the present analysis. Analyzing patients with different
among women, patients in the sarcopenic group were significantly pathologies, such as impaired insulin secretion and insulin resis-
older than those in the non-sarcopenic group, and the duration of tance, might have influenced the results. Fourth, we used a self-
diabetes was longer. Conversely, in men, patients in the sarcope- administered questionnaire in this study, which might have
nic group showed significantly higher insulin resistance than those affected the responses from respondents in the presence of cogni-
in the non-sarcopenic group. Similar results were reported in a tive impairment. Finally, the present study had a cross-sectional
previous study that targeted community-dwelling older patients, design and it is difficult to state a causal relationship. It would be
which showed that a higher degree of muscle loss in men com- necessary to verify a causal relationship in a longitudinal study on
pared with that in women might be associated with increased the association between sarcopenia and sleep disorder in older
insulin resistance in male sarcopenic patients.3 A study that tar- patients with diabetes using SARC-F-J.
geted older people living in an area reported an association Despite the aforementioned limitations, the results of evaluat-
between sarcopenia and sleep disorder.3 Although the exact ing sarcopenia in older patients with diabetes using SARC-F-J,
mechanism underlying the association between sarcopenia and and examining the association between sarcopenia and sleep dis-
sleep disorder remains mostly unknown, the following mecha- order showed that there is a statistically significant association
nisms is possible. Sarcopenia is known to cause insulin resistance between sarcopenia and sleep disorders. It is important to caution
or inflammation.26 Insulin resistance might have a negative impact older patients with diabetes and sarcopenia of sleep disorders.
on the thalamus and suprachiasmatic nucleus (circadian rhythm Further examinations considering the aforementioned limitations
disorder and overactivity of the sympathetic nervous system).27 In are necessary in the future.
the present study, the triglycerides/high-density lipoprotein cho-
lesterol ratio, a surrogate marker of insulin resistance, was higher Acknowledgements
in the sarcopenic group than in the non-sarcopenic group. Insulin
resistance was possibly involved in the association between sarco- The authors thank the staff of the Department of Metabolic Dis-
penia and sleep disorder. A decrease in the level of physical activi- eases at the Ise Red Cross Hospital for their cooperation in this
ties might be another mechanism underlying the association study. This study received no funding.
between sarcopenia and sleep disorders. In other words, a
decrease in the level of physical activities is known to be closely
associated with sarcopenia6 and sleep disorders.3,11 Furthermore,
Disclosure statement
the involvement of endocrine hormones (decrease in insulin-like
growth factors-1 or testosterone and increase in cortisol) in the The authors declare no conflict of interest.
association between sarcopenia and sleep disorders has been sug-
gested.3 In the present study, levels of physical activities and endo- References
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