Clinical Nutrition xxx (2013) 1e5

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Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu

Original article

Prevalence of and factors associated with sarcopenia in elderly patients

with end-stage renal disease
Jwa-Kyung Kim a, d, Sun Ryoung Choi b, d, Myung Jin Choi c, d, Sung Gyun Kim a, d, Young Ki Lee c, d,
Jung Woo Noh c, d, Hyung Jik Kim a, d, Young Rim Song a, d, *
a
Department of Internal Medicine, Hallym University Sacred Heart Hospital, Anyang, Republic of Korea
b
Department of Internal Medicine, Kangnam Sacred Heart Hospital, Seoul, Republic of Korea
c
Department of Internal Medicine, Chuncheon Sacred Heart Hospital, Seoul, Republic of Korea
d
Kidney Research Institute, Hallym University College of Medicine, Republic of Korea

a r t i c l e i n f o s u m m a r y

Article history: Background & aims: We investigated the prevalence of sarcopenia in elderly patients with end-stage renal
Received 17 September 2012 disease (ESRD) and its relationship with various markers of nutrition, cognitive function, depressive
Accepted 2 April 2013 symptoms, inflammation and b2-microglobulin.
Methods: A cross-sectional study was conducted with 95 patients having ESRD aged over 50 years.
Keywords: Sarcopenia was defined as a decline in both muscle mass and strength.
Sarcopenia
Results: The mean age was 63.9
10.0 years; 56.8% were men and 52.6% had diabetes. Sarcopenia was
Inflammation
highly prevalent in elderly patients with ESRD (37.0% in men and 29.3% in women). Subjective Global
Depression
b2-microglobulin Assessment (SGA), inflammatory markers and b2-microglobulin levels were significantly associated with
End-stage renal disease sarcopenia, even after adjustment for age, gender, diabetes, and body mass index. Additionally, patients
with depressive symptoms showed a higher risk of sarcopenia relative to those without depressive
symptoms (odds ratio, OR ¼ 6.87, 95% confidence interval, CI ¼ 2.06e22.96) and sarcopenia was more
likely to be present in patients with mild cognitive dysfunction (OR ¼ 6.35, 95% CI ¼ 1.62e34.96).
Conclusions: Sarcopenia is highly prevalent in elderly patients with ESRD and is closely associated with
SGA, inflammatory markers, b2-microglobulin, depression and cognitive dysfunction.
Ó 2013 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

1. Introduction
Although obesity is associated with an increased risk of mor-
tality in the general population, several observational reports in
patients with end-stage renal disease (ESRD) have suggested the
opposite.1 At the ESRD stage, being overweight or obese is associ-
ated with improved survival whereas being underweight is asso-
ciated with increased mortality, presumably because a high body
mass index (BMI) is usually linked to improved nutrition.2 How-
ever, because being overweight is also linked to inflammation, this
could be a contributing factor in protein-energy wasting (PEW) and
increased mortality in overweight patients with ESRD.3 Moreover,
obesity in patients with ESRD cannot be estimated simply by a high
* Corresponding author. Department of Internal Medicine & Kidney Research
Institute, Hallym University College of Medicine, 896, Pyeongchon-dong, Dongan-
gu, Anyang-si 431-070, Republic of Korea. Tel.: þ82 31 380 3720; fax: þ82 31 386
2269.
E-mail address: yrisong@hanmail.net (Y.R. Song).
BMI because this does not differentiate muscle mass from adipose
tissue mass. Indeed, several studies have demonstrated that the
protective effect conferred by a high BMI seems to be limited to
high muscle mass, not high fat mass.1
Skeletal muscle protein, represented by lean body mass (LBM),
is of particular concern in morbidity and mortality. Reduced muscle
mass, as a common feature of PEW, is an important predictor of
poor outcome in patients with ESRD.4 Additionally, the strength of
skeletal muscle is important. Handgrip strength (HGS) is the most
common method for estimating upper extremity muscle strength.
It may be more useful for patients whose anthropometric mea-
surements fail to distinguish undernourished from underweight
persons, such as those with ESRD. A decline in HGS is closely
associated with an increased length of hospitalization and all-cause
mortality in patients undergoing dialysis.5
Sarcopenia refers to the gradual decline in both muscle quantity
and quality. Initially, it was used to describe the age-related loss of
muscle mass and power. However, recently, it has been recognized
as a syndrome related to various medical conditions because
catabolic inflammatory processes often found in chronic diseases

0261-5614/$ e see front matter Ó 2013 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
http://dx.doi.org/10.1016/j.clnu.2013.04.002

Please cite this article in press as: Kim J-K, et al., Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal
disease, Clinical Nutrition (2013), http://dx.doi.org/10.1016/j.clnu.2013.04.002
2 J.-K. Kim et al. / Clinical Nutrition xxx (2013) 1e5
can enhance the process.6,7 Numerous previous studies have re-
ported the facilitative interaction between pro-inflammatory cy-
tokines and PEW in this patient group, and PEW is regarded as an
important predictor of survival.8 Particularly in patients with ESRD,
uremia-induced anorexia, acidosis, anemia, and hormonal de-
rangements can result in impaired protein assimilation and
aggravated muscle wasting. However, due to a lack of consensus on
the diagnostic criteria of sarcopenia, various methods have been
used to define sarcopenia in patients with ESRD.
In present study, we assessed muscle mass and strength in pa-
tients undergoing hemodialysis, and sarcopenia was defined as a
decline in both muscle mass and strength. We expected sarcopenia
to be more common in elderly patients with ESRD and hypothe-
sized that inflammation, uremic toxins, cognitive dysfunction, and
depression may be associated with sarcopenia. The purpose of this
study was to determine the prevalence of sarcopenia in elderly
patients with ESRD and to evaluate its relationship with various
markers of nutrition, such as BMI, Subjective Global Assessment
(SGA), serum albumin, cognitive function, depressive symptoms,
and b2-microglobulin.
2. Materials and methods
2.1. Study subjects
This observational cross-sectional study was performed in three
dialysis units of Hallym University Sacred Heart Hospital, Korea,
between April 2011 and August 2011. The subjects were 95 elderly
hemodialyis patients who had been maintained for at least 3
months. Elderly patients were defined as aged over 50 years. Pa-
tients were excluded if they met the following criteria: younger
than 50 years, active infection or bleeding within 3 months before
enrollment, a history of malignancy or other chronic inflammatory
disease, and insufficient visual and hearing acuity to complete the
tests. Demographic data, such as age, gender, education, and
financial status, were obtained through patient interviews and later
confirmed from medical records. Baseline comorbid conditions
were scored using the Charlson comorbidity index (CCI). Blood
samples were collected for biochemical determinations immedi-
ately before a mid-week hemodialysis session and plasma was
separated and stored at 80  C until the analysis.
2.2. Nutrition and inflammation status
For the assessment of nutritional status, biochemical analyses
[serum albumin, prealbumin, creatinine, phosphates, high-density
lipoprotein (HDL) cholesterol, low-density lipoprotein (LDL)
cholesterol, triglycerides, and total iron-binding capacity (TIBC)],
SGA, and anthropometric measurement (height, dry weight, BMI,
and triceps skin-fold thickness) were assessed. BMI was calculated
using the following equation of BMI ¼ weight/height2 (kg/m2), and
triceps skin-fold thickness was obtained by one trained clinician
using a Lange Skin-fold Caliper (Beta Technology Inc., Cambridge,
MD, USA) immediately after the hemodialysis session. For SGA, five
components from the medical history (weight change, dietary
intake, gastrointestinal symptoms, functional capacity, comorbid
conditions and its relationship to nutritional requirements) and
three components of a brief physical examination (signs of fat and
muscle wasting, alternations in fluid balance) were used with a
seven-point scoring system.9 High sensitivity C-reactive protein
(hs-CRP) levels were checked using a BN II analyzer (Dade Behring,
Newark, DE, USA) by a latex-enhanced immunonephelometric
method, and serum IL-6 level was measured using with a Quanti-
kine ELISA kit (R&D Systems, Minneapolis, MN, USA).
Please cite this article in press as: Kim J-K, et al., Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal
disease, Clinical Nutrition (2013), http://dx.doi.org/10.1016/j.clnu.2013.04.002
2.3. Depressive symptoms and cognitive function
The Beck Depression Inventory II (BDI-II) consists of 21
multiple-choice questions and scores for each item (range from 0 to
3), with a higher score representing a greater problem. The total
score range is 0e63, in which a score of 0e13 represents minimal
depression, and scores of 14e19, 20e28, and 29 are considered
mild, moderate, and severe depression, respectively. A cutoff score
of 16 was chosen to establish the presence of depression, as in
previous studies.10 To evaluate cognitive status, a brief neuropsy-
chological test, the Mini-Mental State Examination (MMSE) was
used. A cutoff score <24 was chosen to establish the presence of
mild cognitive dysfunction.
2.4. Measurements of muscle mass and strength and assessment of
sarcopenia
The quantification of muscle mass was assessed with a portable
whole-body bioimpedance spectroscopy device (Body Composition
Monitor; Fresenius Medical Care, Bad Homburg, Germany). The
device could provide objective indicators of muscle mass (lean
tissue mass, LTM) as well as fat mass and hydration status. LTM and
fat mass were normalized to the body surface area (m2) to obtain
the Lean Tissue Index (LTI) and Fat Tissue Index (FTI). Low muscle
mass was defined as an LTI of 2 standard deviations (SD) or more
below the normal gender-specific means for young persons. For the
determination of muscle strength, HGS was measured on the non-
fistula hand after a dialysis session using a Jamar handheld dyna-
mometer (JAMAR PLUSþ; Sammons Preston, Inc., Bolingbrook, IL,
USA), which has been established as a reliable measure in
community-dwelling older adults. The subjects stood with both
arms extended sideways from the body with the dynamometer
facing away from the body. Three trials were performed with a rest
period of at least 1 min between trials and the average value was
recorded. Low muscle strength was classified as HGS less than 30
and 20 kg in men and women, respectively.11 Sarcopenia is char-
acterized by decreased skeletal muscle mass and strength with
impaired physical performance. In this study, we adopted the Eu-
ropean Working Group on Sarcopenia in Old People (EWGSOP)
criteria.6 Presarcopenia was defined as having low muscle mass and
normal muscle strength, and sarcopenia was defined as having low
muscle mass combined with low muscle strength.
2.5. Statistical analysis
Statistical analyses were performed using the SPSS software
(ver. 18.0; SPSS Inc., Chicago, IL, USA). All data are expressed as
means
SD or median with ranges. The KolmogoroveSmirnov test
was used to analyze the normality of distribution, and for skewed
data, including serum IL-6 and hs-CRP, natural log values were
used. Pearson’s correlation analysis was used to clarify the re-
lationships between handgrip, LTI, FTI, BDI-II score, and various
clinical and inflammatory parameters. Multiple logistic regression
analysis was performed to find significant determinants of sarco-
penia. p Values <0.05 were deemed to indicate statistical
significance.
3. Results
3.1. Patient characteristics
The subjects in the present study were 95 dialysis patients with
a mean age of 63.9
10.0 (range, 50e88) years; 57.2% (n ¼ 163)
were men and 67.7% (n ¼ 193) had diabetes. Presarcopenia and
sarcopenia were observed in 9 (9.5%) and 32 (33.7%), respectively.
 J.-K. Kim et al. / Clinical Nutrition xxx (2013) 1e5 3

Baseline characteristics of subjects with and without sarcopenia are

shown in Table 1. No significant difference was noted with respect
to age, gender, diabetes, duration of dialysis, BMI, or triceps skin-
fold thickness. Moreover, serum levels of hemoglobin, creatinine,
albumin, prealbumin, and cholesterol were similar. However, sig-
nificant differences were observed in CCI (p ¼ 0.002), financial
status (p ¼ 0.003), SGA (p ¼ 0.027), and BDI-II (p < 0.001) and
MMSE (p ¼ 0.026) scores between the two groups. Serum b2-
microglobulin, hs-CRP, and IL-6 levels were also significantly
higher in patients with sarcopenia than those without, whereas
serum 25-hydroxyvitamin D was significantly lower in this group.
In the patients with diabetes, the HbAlc level was significantly
higher in patients with sarcopenia than those without.

3.2. Correlations between of LTI, HGS, and FTI and various factors

Age-related changes in scores for LTI, FTI, HGS, and MMSE are
Fig. 1. Age-related changes in LTI, FTI, HGS, and MMSE. With increasing age, LTI
shown in Fig. 1. Scores on LTI (p ¼ 0.002), MMSE (p < 0.001), and
(p ¼ 0.002), MMSE (p < 0.001), and HGS (p ¼ 0.002) decreased significantly, but FTI
(p ¼ 0.019) increased significantly. Abbreviations: LTI, lean tissue index; FTI, fat tissue
index; HGS, handgrip strength; MMSE, Mini-Mental State Examination.
Table 1
Baseline characteristics of study subjects.

Variables With sarcopenia Without p Value HGS (p ¼ 0.002) decreased significantly with increasing age. In
(n ¼ 32, 33.7%) sarcopenia contrast, FTI scores increased with increasing age (p ¼ 0.019).
(n ¼ 63, 68.3%)
Correlation analysis between HGS, LTI, and FTI with various clinical
Age (years) 63.4
11.7 64.1
9.3 0.749 factors showed that BMI and triceps skin-fold thickness showed a
Gender, male, n (%) 20 (62.5) 34 (54.0) 0.427
Charlson comorbidity 5.3
3.2 3.1
2.5 0.002
strong association only with FTI, and not with LTI. Conversely, SGA
index (CCI) was closely associated with LTI and HGS, but not with FTI. MMSE
Education, n (%) 0.134 score showed a positive correlation with HGS (r ¼ 345, p ¼ 0.001)
less than high school 6 (18.7) 5 (7.9) and LTI (r ¼ 342, p ¼ 0.001), and a negative association with FTI
graduate
(r ¼ 0.360, p < 0.001). In contrast, the BDI-II score was negatively
high school or higher 26 (81.3) 58 (92.1)
education associated with LTI (r ¼ 0.244, p ¼ 0.017). Inflammatory markers,
Self-reported financial such as hsCRP and IL-6, showed a positive correlation with FTI, but a
status, n (%) negative association with HGS and LTI. Serum level of b2-
no financial problem 21 (65.6) 48 (76.2) 0.003 microglobulin, assessed as a uremic toxin, was associated only
financial difficulties 11 (34.4) 15 (23.8)
Cause of ESRD 0.399
with HGS. Diabetes was also associated only with HGS.
diabetic 20 (62.5) 29 (46.0)
hypertensive 7 (21.9) 21 (33.3)
3.3. Clinical factors associated with sarcopenia
glomerulonephritis 2 (6.3) 8 (12.7)
other 3 (9.4) 5 (7.9)
Duration of dialysis (months) 64.1
43.5 57.1
52.2 0.534 Clinical indicators associated with sarcopenia are presented in
Body mass index (kg/m2) 21.5
2.3 22.7
3.2 0.072 Table 2. After adjusting for age, gender, diabetes, and BMI, the SGA
Triceps muscle thickness (mm) 11.8
3.9 11.2
3.4 0.519 score, CCI, and financial status were independently associated with
SGA 5.6
0.9 6.1
0.7 0.027
Mean arterial pressure (mmHg) 95.9
24.7 101.7
22.8 0.339
BDI-II score 26.6
10.1 17.0
8.8 <0.001
Table 2
MMSE 24.9
4.3 27.0
2.6 0.026
Factors associated with sarcopenia.
Hemoglobin (g/dL) 10.3
1.0 10.0
0.9 0.162
Glucose (mg/dL) 130.9
103.0 100.8
63.5 0.184 Univariate Adjusteda
Albumin (g/dL) 3.7
0.4 3.8
0.3 0.280
Prealbumin (mg/dL) 24.8
10.4 26.2
8.0 0.536 OR 95% CI p OR 95% CI p
HDL-cholesterol (mg/dL) 44.4
1.6 43.7
10.2 0.807 Age 0.99 0.95e1.04 0.746 e e e
LDL-cholesterol (mg/dL) 76.3
28.4 80.5
20.6 0.464 Gender 0.98 0.99e1.01 0.969 e e e
Triglyceride (mg/dL) 100.8
55.5 83.8
43.6 0.152 Diabetes 2.45 0.97e6.20 0.058 e e e
Serum ferritin (mg/L) 204.2
157.0 204
114.1 0.996 BMI (kg/m2) 0.854 0.717e1.017 0.077 e e e
Intact PTH (pg/mL) 188.7
328.7 146.7
1.4.3 0.394 SGA 0.43 0.22e0.85 0.020 0.30 0.14e0.65 0.002
b2-microglobulin (mg/L) 29.9
7.3 23.7
7.0 0.002 Financial status 4.31 1.37e13.55 0.012 10.33 2.44e43.81 0.002
25-hydroxyvitamin D 7.9
4.2 10.4
5.2 0.048 CCI 1.33 1.08e1.63 0.007 1.40 1.11e1.76 0.004
IL-6* 8.8 (1.5e110.5) 3.2 (0.2e109.6) 0.003 hs-CRPb 1.86 1.20e2.87 0.006 2.13 1.28e3.54 0.004
hsCRP* 2.3 (0.1e75.5) 0.8 (0.1e59.6) 0.002 IL-6b 2.32 1.26e4.29 0.007 2.35 1.21e4.58 0.012
HbA1c 7.4
1.3 6.7
1.0 0.038 b2-microglobulin 1.14 1.04e1.24 0.005 1.14 1.04e1.26 0.005
spKt/V 1.6
0.3 1.5
0.2 0.182 Depression 8.75 2.74e27.90 <0.001 6.87 2.06e22.96 0.002
nPCR (g/kg/day) 1.1
0.3 1.1
0.3 0.547 Cognitive 4.37 1.41e13.51 0.011 6.35 1.62e34.96 0.008
dysfunction
All data are expressed as means
SD except for those with, * which are expressed as
median with range. Abbreviations: OR, odds ratio; BMI, body mass index; SGA, Subjective Global
Abbreviations: SGA, Subjective Global Assessment; BDI-II, Beck Depression In- Assessment; CCI, Charlson comorbidity index; hs-CRP, high sensitivity C-reactive
ventory II; MMSE, Mini-Mental State Examination; HDL, high-density lipoprotein protein; IL-6, interleukin-6.
a
cholesterol; LDL, low-density lipoprotein cholesterol; intact PTH, intact parathyroid Multivariate logistic analysis was performed after adjusting for age, gender, BMI,
hormone; IL-6, interleukin-6; hs-CRP, high sensitivity C-reactive protein; spKt/V, diabetes.
b
single pool Kt/V; nPCR, normalized protein catabolism rate. Log-transformed value.

Please cite this article in press as: Kim J-K, et al., Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal
disease, Clinical Nutrition (2013), http://dx.doi.org/10.1016/j.clnu.2013.04.002
4 J.-K. Kim et al. / Clinical Nutrition xxx (2013) 1e5
the presence of sarcopenia. Among serum markers, hsCRP, IL-6, and
b2-microglobulin were significantly associated with sarcopenia.
Sarcopenia was significantly associated with the BDI-II score and
patients with depressive symptoms showed a higher risk of sar-
copenia versus those without depressive symptoms (OR ¼ 6.87, 95%
CI ¼ 2.06e22.96; p ¼ 0.002). Similarly, sarcopenia was significantly
associated with the MMSE score and was more likely to be present
among patients with mild cognitive dysfunction (MMSE < 24,
OR ¼ 6.35, 95% CI ¼ 1.62e34.96; p ¼ 0.008).
4. Discussion
The primary findings of present study are that sarcopenia,
defined according to the EWGSOP criteria, is highly prevalent in
elderly patients with ESRD (37.0% in men and 29.3% in women
patients); common nutritional surrogates, such as BMI, triceps
skin-fold thickness, serum albumin, and prealbumin, were not
associated with the presence of sarcopenia; BMI and triceps skin-
fold thickness were associated with FTI, but not with LTI or HGS;
SGA, inflammatory markers, b2-microglobulin, financial status,
comorbidity (CCI), depression, and cognitive function were asso-
ciated with the presence of sarcopenia, even after adjustment for
age, gender, diabetes, and BMI.
Sarcopenia is a syndrome characterized by the progressive loss
of muscle mass and strength.6 Initially, the term “sarcopenia” was
introduced by Rosenberg to describe the age-related progressive
loss of muscle mass (primary sarcopenia as a geriatric syndrome).7
Recently, debate has occurred as to whether sarcopenia should
include all other forms of muscle wasting related to chronic med-
ical diseases, endocrine derangement, starvation, immobilization,
or cachexia (secondary sarcopenia). With this concept, it may be a
clinical-care target for many pathological conditions. Indeed,
growing evidence suggests that sarcopenia is related to adverse
clinical outcomes, both in the general population and in patients
with renal dysfunction.6,12 According to a recently published pro-
spective study, reduced physical activity was relatively common in
CKD patients and it increased risk of death or renal progression.13.14
In this study, we evaluated the prevalence of sarcopenia and its
relationship with various clinical markers in a comprehensive way.
According to our data, among nutritional markers, only SGA was
significantly associated with sarcopenia. SGA is a clinical scoring
system taking into account both subjective and objective factors.
The role of SGA in patients with ESRD has been widely validated,
and the Kidney Disease/Dialysis Outcomes and Quality Initiative (K/
DOQI) recommends its use in nutritional assessment of the adult
dialysis population.9 A one-unit decrease in SGA increased the
mortality of patients undergoing continuous ambulatory peritoneal
dialysis (CAPD) by 25%.15 However, BMI and serum albumin,
traditionally known as nutritional markers, were not related to
sarcopenia in our study. BMI was positively correlated with triceps
skin-fold thickness and FTI, but not associated with HGS or LTI,
revealing that increased fat tissue mass essentially explained the
higher BMI. Generally, BMI is well correlated with the amount of
body fat. However, Torun and colleagues reported that increased
BMI was not a reliable marker of good nutrition in hemodialysis
patients.16 In fact, in our study, not all patients with sarcopenia
displayed a lower BMI (median: 20.9; range: 17.20e29.90), and
only 48.4% of those patients had a BMI less than 20 (i.e., were un-
derweight). Similarly, we did not identify any association between
serum (pre)albumin and sarcopenia. Serum (pre)albumin levels
also showed no correlation with LTI, HGS, or FTI. This finding is not
surprising, considering that the serum albumin level may not be a
reliable marker for nutritional status; rather, it is more a marker of
inflammation.17 Although several studies have reported that low
serum albumin levels reflected poor nutritional status and were
Please cite this article in press as: Kim J-K, et al., Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal
disease, Clinical Nutrition (2013), http://dx.doi.org/10.1016/j.clnu.2013.04.002
strongly associated with mortality, its predictive power decreased
when the effect of inflammation was accounted for using multi-
variate analysis. Clearly, in the clinical setting of anorexia and sar-
copenia, hypoalbuminemia and inflammation occur together and
are difficult to differentiate.
However, chronic inflammation was an important factor
affecting sarcopenia in patients with ESRD. Elevated IL-6 and hs-
CRP levels were associated with decreased muscle mass and
strength, and a one-unit increase in those markers was linked with
at least a twofold increased risk of sarcopenia. Previous studies
have reported that higher levels of pro-inflammatory cytokines
contributed to increased lipolysis, muscle protein breakdown, and
nitrogen loss, leading to sarcopenia and increased mortality in
these patients.18 Elevated levels of tumor necrosis factor-a (TNF-a)
are associated with anorexia in peritoneal dialysis patients,19 and
IL-6 has been shown to stimulate muscle catabolism and increase
mortality.20
Depression and cognitive dysfunction may be another causative
factor for sarcopenia in patients with ESRD. According to a large-
scale study with an elderly population, depressed mood was a
strong predictor of a rapid decrease in HGS.21 In patients with a
decreased physiological capacity due to chronic conditions, such as
the ESRD population, the effects of depressed mood may be much
greater and could significantly decrease the muscle mass and
strength.22e24 Additionally, many clinical studies have suggested a
close association between depression and inflammatory status.
Particularly in dialysis patients, depression is considered as part of
“malnutrition-inflammation atherosclerosis” syndrome (MIA syn-
drome).25e28
Although the mechanism(s) remain(s) incompletely under-
stood, it is likely that advanced malnutrition and inflammation,
with its attendant disability and loss of independence, become a
possible cause of depression. In combination with cognitive
dysfunction, often found in elderly patients with uremia,
depression may be an indicator of chronic PEW in patients with
ESRD and could be an important predisposing factor for
sarcopenia.23
The present study has several limitations. First, because the BDI-
II is a self-reported inventory, scores may have been affected by
such factors as social desirability. Additionally, those with
concomitant physical illnesses may have inflated scores due to the
test’s reliance on physical symptoms, including fatigue. This may
have artificially inflated scores due to illness-related symptoms
rather than to depression per se. Second, only 95 dialysis patients
were evaluated in the present study, which resulted in wide con-
fidence intervals around predictions. Third, the prevalence of
depression in the present study was relatively high compared with
that in previous studies. This may be due to the higher comorbidity
index in our subjects. Finally, as a cross-sectional study, causal re-
lationships between sarcopenia and risk factors could not be
determined.
In conclusion, sarcopenia is highly prevalent in elderly patients
with ESRD and is closely associated with SGA, comorbidity index,
inflammatory markers, b2-microglobulin, and depression and
cognitive dysfunction.
Statement of authorship
The contributions of the authors to the manuscript are as fol-
lows. YR Song: study design, data analysis and writing of the
manuscript; JK Kim: data collection and writing of the manuscript;
SR Choi and MJ Choi; data collection; SG Kim and HJ Kim: data
analysis and reviewing the manuscript; YK Lee and JW Noh:
reviewing the manuscript. All authors read and approved the
manuscript.
 J.-K. Kim et al. / Clinical Nutrition xxx (2013) 1e5
Conflict of interest
No financial conflict of interest was involved in this study.
The acknowledgment
The English in this document has been checked by at least two
professional editors, both native speakers of English. For a certifi-
cate, please see: http://www.textcheck.com/certificate/POcR3i.
References
1. Mafra D, Guebre-Egziabher F, Fouque D. Body mass index, muscle and fat in
chronic kidney disease: questions about survival. Nephrol Dial Transplant
2008;23:2461e6.
2. Fleischmann E, Teal N, Dudley J, May W, Bower JD, Salahudeen AK. Influence of
excess weight on mortality and hospital stay in 1346 hemodialysis patients.
Kidney Int 1999;55:1560e7.
3. Honda H, Qureshi AR, Axelsson J, Heimburger O, Suliman ME, Barany P, et al.
Obese sarcopenia in patients with end-stage renal disease is associated with
inflammation and increased mortality. Am J Clin Nutr 2007;86:633e8.
4. Thomas DR. Loss of skeletal muscle mass in aging: examining the relationship
of starvation, sarcopenia and cachexia. Clin Nutr (Edinburgh, Scotland) 2007;26:
389e99.
5. Chang YT, Wu HL, Guo HR, Cheng YY, Tseng CC, Wang MC, et al. Handgrip
strength is an independent predictor of renal outcomes in patients with
chronic kidney diseases. Nephrol Dial Transplant 2011;26:3588e95.
6. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al.
Sarcopenia: European consensus on definition and diagnosis: report of the
European Working Group on Sarcopenia in older people. Age Ageing 2010;39:
412e23.
7. Rosenberg IH. Sarcopenia: origins and clinical relevance. Clin Geriatr Med
2011;27:337e9.
8. Stenvinkel P, Lindholm B, Heimburger O. Novel approaches in an integrated
therapy of inflammatory-associated wasting in end-stage renal disease. Semin
Dial 2004;17:505e15.
9. Steiber AL, Kalantar-Zadeh K, Secker D, McCarthy M, Sehgal A, McCann L.
Subjective global assessment in chronic kidney disease: a review. J Ren Nutr
2004;14:191e200.
10. Chilcot J, Norton S, Wellsted D, Almond M, Davenport A, Farrington K.
A confirmatory factor analysis of the Beck depression inventory-ii in end-stage
renal disease patients. J Psychosom Res 2011;71:148e53.
11. Landi F, Liperoti R, Fusco D, Mastropaolo S, Quattrociocchi D, Proia A, et al.
Prevalence and risk factors of sarcopenia among nursing home older residents.
J Gerontol Ser A 2012;67:48e55.
Please cite this article in press as: Kim J-K, et al., Prevalence of and factors associated with sarcopenia in elderly patients with end-stage renal
disease, Clinical Nutrition (2013), http://dx.doi.org/10.1016/j.clnu.2013.04.002
5
12. Noori N, Kopple JD, Kovesdy CP, Feroze U, Sim JJ, Murali SB, et al. Mid-arm
muscle circumference and quality of life and survival in maintenance hemo-
dialysis patients. Clin J Am Soc Nephrol 2010;5:2258e68.
13. Roshanravan B, Khatri M, Robinson-Cohen C, Levin G, Patel KV, de Boer IH, et al.
A prospective study of frailty in nephrology-referred patients with CKD. Am J
Kidney Dis 2012;60:912e21.
14. Wilhelm-Leen ER, Hall YN, K Tamura M, Chertow GM. Frailty and chronic
kidney disease: the Third National Health and Nutrition Evaluation Survey. Am
J Med 2009;122:664e71.
15. Anonymous. Adequacy of dialysis and nutrition in continuous peritoneal
dialysis: association with clinical outcomes. Canada-USA (CANUSA) Peritoneal
Dialysis Study Group. J Am Soc Nephrol 1996;7:198e207.
16. Torun D, Micozkadioglu H, Torun N, Ozelsancak R, Sezer S, Adam FU, et al.
Increased body mass index is not a reliable marker of good nutrition in he-
modialysis patients. Ren Fail 2007;29:487e93.
17. Friedman AN, Fadem SZ. Reassessment of albumin as a nutritional marker in
kidney disease. J Am Soc Nephrol 2010;21:223e30.
18. Meuwese CL, Carrero JJ, Stenvinkel P. Recent insights in inflammation-
associated wasting in patients with chronic kidney disease. Contrib Nephrol
2011;171:120e6.
19. Aguilera A, Codoceo R, Selgas R, Garcia P, Picornell M, Diaz C, et al. Anorexigen
(TNF-alpha, cholecystokinin) and orexigen (neuropeptide Y) plasma levels in
peritoneal dialysis (PD) patients: their relationship with nutritional parame-
ters. Nephrol Dial Transplant 1998;13:1476e83.
20. Ershler WB. A gripping reality: oxidative stress, inflammation, and the pathway
to frailty. J Appl Physiol (Bethesda, MD: 1985) 2007;103:3e5.
21. Rantanen T, Penninx BW, Masaki K, Lintunen T, Foley D, Guralnik JM.
Depressed mood and body mass index as predictors of muscle strength decline
in old men. J Am Geriatr Soc 2000;48:613e7.
22. Finkelstein FO, Finkelstein SH. Depression in chronic dialysis patients: assess-
ment and treatment. Nephrol Dial Transplant 2000;15:1911e3.
23. Cohen SD, Norris L, Acquaviva K, Peterson RA, Kimmel PL. Screening, diagnosis,
and treatment of depression in patients with end-stage renal disease. Clin J Am
Soc Nephrol 2007;2:1332e42.
24. Bowling CB, Muntner P. Epidemiology of chronic kidney disease among older
adults: a focus on the oldest old. J Gerontol A Biol Sci Med Sci 2012;67:1379e86.
25. Czira ME, Lindner AV, Szeifert L, Molnar MZ, Fornadi K, Kelemen A, et al.
Association between the malnutrition-inflammation score and depressive
symptoms in kidney transplanted patients. Gen Hosp Psychiatry 2011;33:
157e65.
26. Kalender B, Ozdemir AC, Koroglu G. Association of depression with markers of
nutrition and inflammation in chronic kidney disease and end-stage renal
disease. Nephron Clin Pract 2006;102:c115e21.
27. Bilgic A, Akgul A, Sezer S, Arat Z, Ozdemir FN, Haberal M. Nutritional status and
depression, sleep disorder, and quality of life in hemodialysis patients. J Ren
Nutr 2007;17:381e8.
28. Simic Ogrizovic S, Jovanovic D, Dopsaj V, Radovic M, Sumarac Z, Bogavac SN,
et al. Could depression be a new branch of MIA syndrome? Clin Nephrol
2009;71:164e72.