Nephrol Dial Transplant (2010) 25: 2662–2671
doi: 10.1093/ndt/gfq031
Advance Access publication 26 February 2010
Objective Score of Nutrition on Dialysis (OSND) as an alternative for
the malnutrition–inflammation score in assessment of nutritional risk
of haemodialysis patients
Ilia Beberashvili1, Ada Azar2, Inna Sinuani1, Hila Yasur2, Leonid Feldman1, Zhan Averbukh1
and Joshua Weissgarten1
1
Nephrology Division, Assaf Harofeh Medical Center, Zerifin, Affiliated to Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv,
Israel and 2Nutrition department, Assaf Harofeh Medical Center, Zerifin, Affiliated to Sackler Faculty of Medicine, Tel Aviv
University, Tel Aviv, Israel
Correspondence and offprint requests to: Ilia Beberashvili; E-mail: iliab@asaf.health.gov.il
Abstract
Background. Evaluation of nutritional risk, one of the
strongest predictors of morbidity and mortality in mainten-
ance haemodialysis (HD) patients, is a difficult process es-
pecially in patients with compounding conditions that
prevent subjective assessment by subjective global assess-
ment or malnutrition–inflammation score (MIS).
Methods. In this study, we developed and characterized a
score for the assessment of nutritional status in dialysis pa-
tients based solely on objectively measurable criteria. Our
prospective observational cohort included 81 prevalent
HD patients (53 men and 28 women) with a mean age of
64.3 ± 11.9 years. The study period encompassed 26.9 ±
14.3 months. The quantitative and comprehensive scoring
system, named Objective Score of Nutrition on Dialysis
(OSND), was calculated by combining anthropometric
measurements (the change in end-dialysis dry weight in
the past 3–6 months, body mass index, skinfold thickness
and mid-arm circumference) with three laboratory tests:
albumin, transferrin and cholesterol levels. The sum of
all seven components of OSND results in a score from
5 (severely malnourished) to 32 (normal). We compared
our OSND system with the accepted MIS and phase
angle (PA) measurements derived by bioelectric imped-
ance analysis.
Results. The OSND correlated signif icantly with
hospitalization days (r = −0.334; P = 0.002) and frequency
of hospitalization (r = −0.373; P = 0.001), as well as with
lean body mass and fat mass, MIS, PA and interleukin-6
levels. The Cox proportional hazard-calculated relative
risk for death for each five-unit decrease in the OSND
was 2.2 (95% CI, 1.3 to 3.8; P = 0.003) comparable with
the predictions provided by MIS [for each five-unit in-
crease in MIS, hazard ratio (HR) was 1.8 with 95% CI,
1.2 to 2.8; P = 0.007] and PA (for each 1-unit decrease
in PA, HR was 2.9 with 95% CI, 1.5 to 5.6; P = 0.001).
Conclusions. The OSND thus provides a comprehensive
scoring system with significant associations with prospect-
ive hospitalization and mortality in chronic HD patients as
well as measures of nutrition and inflammation.
© The Author 2010. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved.
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Keywords: bioelectric impedance; haemodialysis; inflammation;
malnutrition–inflammation score; nutrition
Introduction
The presence of protein-energy malnutrition (PEM) is
one of the strongest predictors of morbidity and mortal-
ity in end-stage renal disease (ESRD) patients receiving
maintenance haemodialysis (HD) therapy [1,2]. The sub-
jective global assessment (SGA) was designed for evalu-
ation of nutritional status on the basis of the history and
physical examination [3]. It was found to be reliable and
valid for assessing PEM in a dialysis population [4,5],
and since 2000 the National Kidney Foundation Kidney
Disease/Dialysis Outcomes and Quality Initiative (K/
DOQI) has recommended the use of the SGA for asses-
sing the nutritional status of such patients [6]. However,
its semiquantitative scoring (it consists of only three nu-
tritional levels—normal, mild to moderate and severe) and
the subjective nature of the SGA may limit its reliability.
When compared with total-body nitrogen (TBN) level, the
gold standard for nutrition, SGA was able to differentiate
severely malnourished patients from those with normal nu-
trition, but it was not a reliable predictor of the degree of
malnutrition [7]. This led to the development of a fully
quantitative scoring system—a modified SGA or dialysis
malnutrition score [8] and, further, of a malnutrition–in-
flammation score (MIS) by Kalantar-Zadeh et al. [9,10].
MIS has been validated as a better nutritional indicator than
the SGA [9] and was reported to correlate with morbidity,
mortality, various nutritional variables, inflammation
[9,10], anaemia and erythropoietin hyporesponsiveness in
maintenance haemodialysis patients [11]. Still, MIS is
based on the SGA and therefore requires subjective assess-
ment and judgment by the examiner. Several factors (such as
mental disabilities of ESRD patients or acute gastrointes-
tinal pathology, independent of ongoing nutritional factors)
may significantly impact MIS scoring without adversely af-
Nutritional risk assessment of haemodialysis patients
fecting nutrition. The prevalence of global cognitive impair-
ment in persons with end-stage renal disease, reported as
more than twice that of the age-matched general population,
was not explained by commonly measured metabolic altera-
tions associated with kidney disease [12,13]. Nutritional
evaluation of these patients by MIS may be difficult and
can yield equivocal results. Thus, only objective methods
of assessment are useful in this setting.
It is recognized that no single alternative objective test is
able to determine the overall nutritional status in patients
with ESRD. Although some attributes of nutritional status
such as serum albumin [14,15], cholesterol [16] or trans-
ferrin [17], anthropometric indexes [18,19], dual-energy
X-ray absorptiometry (DEXA) [20] or bioelectrical imped-
ance analysis (BIA) nutritional indexes [21,22] correlate
with clinical outcome, it is not clear which, if any of these
measurements has a predictably superior outcome when
compared with others. Nutritional assessment by different
individual methods may sometimes lead to conflicting re-
sults. Moreover, most of these methods may be affected to
some degree by factors inherent in renal failure, mode and
adequacy of dialysis delivery, and fluid status at the time of
assessment. Therefore, a scoring system that relies on a
series of objective measurements may provide a more
powerful tool in assessment of overall nutritional status
of chronic HD patients.
The aim of this study was to develop a simple, reliable
and valid malnutrition scoring system based only on rou-
tine objective measurements. The present report describes
such a system and our attempts to validate it in chronic HD
patients by comparing it with conventional measures of
nutritional state, including blood tests, anthropometry,
MIS and bioelectric impedance analysis and several mea-
sures of clinical outcome including prospective mortality
and hospitalization.
Materials and methods
Patients
This prospective observational study was approved by the Ethics Commit-
tee of Assaf Harofeh Medical Center (Zerifin, Affiliated to the Sackler
Faculty of Medicine Tel Aviv University, Israel). Informed consent was
obtained before any trial-related activities. Patients were eligible for entry
when they had been on HD therapy for at least 3 months and were 18
years or older, with no clinically active cardiovascular or infectious dis-
eases on entry. We excluded patients with oedema, pleural effusion or as-
cites at their initial assessment, as well as patients with malignant disease,
liver cirrhosis, neuromuscular diseases, amputations or any deformities of
the body. As a whole, 100 patients were screened for eligibility for the
trial; 13 were excluded because they did not fully meet inclusion criteria,
and six withdrew their informed consent before enrollment. In total, 81
patients (53 men and 28 women), with a mean age 64.3 ± 11.9 years,
receiving maintenance haemodialysis treatment at our outpatient HD in-
stitution (Division of Nephrology, Assaf Harofeh Medical Center, Zerifin,
Affiliated to Sackler Faculty of Medicine Tel Aviv University, Israel) were
included in the study. Of the patients studied, 44 were diabetic (all of
whom suffered from type 2 diabetes). The study period extended 26.9
± 14.3 months. During this period, 22 patients (22.7%) died [the main
causes of death were cardiovascular (8 of 22 patients; 36.4%) and septic
(7 of 22 patients; 31.8%) disorders], 10 patients (12.3%) underwent kid-
ney transplantation, 3 patients (3.7%) changed dialysis modality and 8
patients (9.9%) were transferred to other haemodialysis units. Thus, 21
patients were censored from the time of their transplantation or transfer
to another haemodialysis or peritoneal dialysis unit. In total, 38 patients
completed the study. All patients underwent regular dialysis via their vas-
2663
cular access (82.7% of patients had arterio-venous fistula) 4–5 h three
times per week at a blood flow rate of 250–300 ml/min. Bicarbonate di-
alysate (30 mEq/l) at a dialysis solution flow rate of 500 ml/min was used
in all cases. All dialysis was performed with biocompatible dialyser mem-
brane with a surface area of 1.0–1.8 m2. The efficiency of the dialysis was
assessed based on the delivered dose of dialysis (Kt/V urea) using a sin-
gle-pool urea kinetic model (mean Kt/V was1.3 ± 0.25 in our population).
Information on vascular disease (cerebral vascular, peripheral vascular
and heart disease) was obtained from a detailed medical history.
Most patients were taking antihypertensive medications as well as
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other drugs commonly used in ESRD, such as phosphate and potassium
binders, diuretics, and supplements of vitamins B, C and D.
Malnutrition–inflammation score
MIS, a comprehensive scoring system with significant associations with
prospective hospitalization and mortality as well as measures of nutrition,
inflammation and anaemia in HD patients, has been described in detail in
several recent prospective studies [9,10]. It consists of four sections [nutri-
tional history, physical examination, body mass index (BMI) and laboratory
values] and 10 components. Each MIS component has four levels of severity
from 0 (normal) to 3 (very severe). The sum of all 10 components results in
an overall score ranging from 0 (normal) to 30 (severely malnourished).
Objective Score of Nutrition on Dialysis
In an attempt to develop a scoring system free of subjective assessments
(that required judgment by the examiner), we created the Objective Score
of Nutrition on Dialysis (OSND) by combining the change in end-dialysis
dry weight (overall change in the past 3–6 months) with anthropometric
measurements (BMI, skinfold thickness and mid-arm circumference) and
three laboratory tests (serum albumin, transferrin and total cholesterol).
Thus, the Objective Score of Nutrition on Dialysis has seven components.
Each of these components is categorized into three malnutrition risk cat-
egories (normal, moderate and low); a lower score reflects a more severe
degree of malnutrition.
Table 1 shows the scoring sheet developed, consisting of the seven
elements.
Weight change is determined as the change in oedema-free body weight
obtained after haemodialysis sessions over the course of 6 months. The
lowest score 1 is given if weight loss is 10% or greater. A score of 2 indi-
cates weight loss that is between 5% and 10% of dry weight. A score of 4 is
given for weight loss <5% of body weight or any increase in body weight.
Body mass index was also grouped into three categories: BMI <17 kg/
m2 is scored as 1, BMI between 17 and 19.9 kg/m2 is scored as 2 and
normal BMI (≥20 kg/m2) is scored as 4.
Triceps skinfold thickness (TSF) is scored 1 if it is <9.9 mm for males
and <13.1 mm for females. A score of 2 is given if TSF is 10.0–12.4 mm
for males and 13.2–16.4 mm for females; and score 4 is given if TSF is
above 12.5 mm for males and 16.5 mm for females.
Mid-arm circumference (MAC) is scored 1 if it is <20.1 cm for males
and <18.5 cm for females; 2 if MAC is 20.2–25.2 cm for males and 18.6–
23.1 cm for females; and 4 if MAC is above 25.3 cm for males and 23.2
cm for females.
The OSND includes three laboratory values. Hypoalbuminaemia <3.0
g/dL is scored as 0, serum albumin 3.1–3.4 g/dL is scored as 3 and nor-
moalbuminaemia (serum albumin above 3.5 g/dL) is scored as 6.
Serum total cholesterol level is scored 0 when it is <150 mg/dL; 3 if
serum cholesterol is 150–200 mg/dL; and 6 if serum cholesterol is above
200 mg/dL. For haemodialysis patients also treated with statins, a choles-
terol level <130 mg/dL (instead of 150 mg/dL) is scored as 0; cholesterol
130–180 mg/dL is scored as 3 in such patients, and cholesterol level
above 180 mg/dL is scored as 6.
Note that we score serum albumin and cholesterol levels by the 0, 3, 6
system instead of the 1, 2, 4 system (used for the other indicators). This
gives albumin and cholesterol levels greater weight, corresponding to
their profound impact on outcome of haemodialysis patients [14–16].
Serum transferrin is scored 1 when its level is <120 mg/dL; 2 if
serum transferrin is 120–149 mg/dL; and 4 if serum transferrin is above
150 mg/dL.
The sum of all seven components ranges from 32 (normal) to 5 (se-
verely malnourished). The OSND can be used to stratify haemodialysis
patients into three nutritional status categories. Using our system, a score
of 28–32 indicates normal nutritional status of the patient; a score of 23–
2664 I. Beberashvili et al.
Table 1. Components of Objective Score of Nutrition on Dialysis (OSND)

Nutritional parameters Normal Moderate Low

Decrease in dry weight (in the past 3–6 months) 4 2 1

Male (%) <5 5–10 >10
Female (%) <5 5–10 >10
BMI [BMI=Wt(kg)/Ht2(m)] 4 2 1
Male (kg/m2) >19 16.5–18.5 <16.4
Female (kg/m2) >20 17–19.9 <16.9

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TSF (mm) 4 2 1
Male >12.5 10.0–12.4 <9.9
Female >16.5 13.2–16.4 <13.1
MAC (cm) 4 2 1
Male >25.3 20.2–25.2 <20.1
Female >23.2 18.6–23.1 <18.5
Transferrin (mg/dL) 4 2 1
Male >150 120–149 <120
Female >150 120–149 <120
Albumin (g/dL) 6 3 0
Male 3.5–5.0 3.1–3.4 <3.0
Female 3.5–5.0 3.1–3.4 <3.0
Cholesterol (mg/dL)a 6 3 0
Male >200 150–200 <150
Female >200 150–200 <150
Total score (sum of all 8 components) 32 16 5
Nutritional status 28–32 23–27 ≤22

BMI, body mass index; Wt, weight; Ht, height; TSF, triceps skinfold thickness; MAC, mid-arm circumference.
a
For haemodialysis patients also treated with statins, a cholesterol level <130 mg/dL (instead of 150 mg/dL) is scored as 0; cholesterol 130–180 mg/dL
is scored as 3 in such patients and cholesterol level above 180 mg/dL is scored as 6.

27 indicates moderate nutritional risk, and a score of <22 indicates an
unsatisfactory nutritional status of haemodialysis patients.
Anthropometric measurements
All measurements were made after dialysis when the patient was at dry
weight (the right upper arm was used whenever possible, with exceptions
made for patients in whom dialysis access placement, injury or stroke
precluded measurement). The same dietitian performed all anthropomet-
ric measurements. BMI, TSF, MAC and calculated mid-arm muscle cir-
cumference (MAMC) were measured as anthropometric variables. The
BMI was calculated as dry weight in kilograms divided by the square
of height in meters. TSF was measured with a conventional skinfold cali-
per using standard techniques. Mid-arm circumference was measured
with a plastic measuring tape. MAMC was estimated as follows: MAMC
(cm) = mid-arm circumference (cm) − 0.314 × TSF (mm).
Anthropometric norms for dialysis patients were previously reported
[6,23,24].
Hospitalization was defined as any hospital admission that included at
least one overnight stay in the hospital. The admission day was counted
as one full hospitalization day, but the discharge day was not. The sum of
all hospitalization days of a given patient during the study period was
defined as the hospitalization days. The hospitalization frequency was
the total number of hospital admissions during the same period irrespect-
ive of the length of each admission. Any access-related hospitalizations
were not included in hospitalization data.
Laboratory evaluation
Blood samples were taken before starting a dialysis session. CBC, creatin-
ine, urea, albumin, transferrin and total cholesterol were measured by rou-
tine laboratory methods. IL-6 was measured in plasma samples using
commercially available enzyme-linked immunosorbent assay (ELISA)
kits (R&D System, Minneapolis, MN, USA) according to the manufac-
turer’s protocol. The mean minimal detectable dose (mean MDD) for IL-6
was 0.7 pg/mL.

Body composition analysis Statistical analysis

Body composition was determined by body impedance analysis (B.I.A.
Nutriguard-M, Data-Input, Frankfurt, Germany). We used gel-based elec-
trodes specifically developed for BIA measurements—Bianostic AT
(Data-Input GmbH). On the day of blood collection, patients underwent
BIA measurement at approximately 30 min postdialysis. BIA electrodes
were placed on the same body side used for anthropometric measure-
ments. The multi-frequency technique was used. The validity of BIA in
HD patients was proven using deuterium oxide and sodium bromide iso-
tope dilution studies [25,26]. Fat-free mass (FFM) was calculated by
using the approach of Kyle et al. validated by dual-energy X-ray absorp-
tiometry on 343 healthy adult subjects [27]:
FFM = −4:104 + ð0:518 × height2 =resistanceÞ
+ ð0:231 × weightÞ + ð0:130 × reactanceÞ
+ ð4:229 × sex : men = 1; women = 0Þ:
Hospitalization
Patients were followed up prospectively for up to 2 years after starting the
study, and hospitalization data were obtained for all 81 HD patients.
Results were expressed as mean values ± SD or as median and range for
variables that did not follow a normal distribution.
Univariate analysis was performed to identify risk factors that were
statistically related to morbidity and mortality. Variables identified from
the univariate analysis as potential predictors were included in the multi-
variate analysis. The P-value for entry into the model was 0.05 and for
removal 0.1. The cutoff values of variables were based on the distribution
within the cohort. Multiple logistic regression was used to provide adjusted
odds ratios and 95% confidence intervals (CI) for each independent risk
factor. These were subsequently used as weights in the derivation of the
OSND. The final coefficients produced were then altered by rounding to
integer values to create a more easily applicable and clinically usable scor-
ing system. The cutoffs for the most accurate discrimination of nutritional
risk according to OSND were derived from the receiver operating charac-
teristic (ROC) area under the ROC curve (AUC).
To compare the means of continuous variables measured between sub-
groups of severity of the OSND, one-way analysis of variance (ANOVA)
and analysis of covariance with adjustments. Analysis of covariance (AN-
COVA) was used. Categorical data are presented as percentages and were
compared among groups by χ2 tests. Correlations between OSND and
Nutritional risk assessment of haemodialysis patients 2665
Table 2. Demographic, clinical and nutritional variables for 81 chronic HD patients as classified by OSND

Objective Score of Nutrition on Dialysis

All patients 28–32 23–27 ≤22
Variables (n = 81) (n = 18) (n = 48) (n = 15) ANOVA ANCOVA

Demography
Gender (male/female)a 65.4/34.6 66.7/33.3 64.6/35.4 66.7/33.3 NS –
Age (years) 64.3 ± 11.9 64.9 ± 11.3 63.2 ± 11.1 67.2 ± 14.9 NS –

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DM a 54.3 61.1 58.3 33.3 NS –
History of cardiovascular disease a
51.9 55.6 45.8 66.7 NS –
Dialysis vintage (months) 27 (3–183) 32.0 (5–88) 30.8 (3–123) 30.0 (5–183) NS NSb
Hospitalization daysc 8.0 (0–87) 3.5 (0–30) 7.5 (0–87) 20.0 (2–63) 0.014 0.010b
Frequency of hospitalizationc 2.0 (0–14) 1.5 (0–6) 2.0 (0–14) 4.0 (1–7) 0.022 0.018b
Anthropometric measurements
BMI (kg/m2) 28.3 ± 5.6 30.3 ± 4.2 29.1 ± 5.7 23.2 ± 3.8 0.001 0.001b
TSF (mm) 17.4 ± 6.6 21.3 ± 4.6 18.5 ± 6.9 11.7 ± 4.4 0.0001 0.0001b
MAC (cm) 28.2 ± 3.4 30.8 ± 2.6 28.2 ± 3.1 24.6 ± 2.7 0.0001 0.0001b
MAMC (cm) 23.3 ± 2.4 24.1 ± 2.0 23.7 ± 2.3 21.5 ± 2.7 0.003 0.002b
Blood analysis
nPNA 1.03 ± 0.26 1.03 ± 0.23 1.05 ± 0.26 0.98 ± 0.30 NS NSb
Kt/V 1.3 ± 0.25 1.30 ± 0.22 1.28 ± 0.22 1.52 ± 0.31 0.003 0.005b
Albumin (g/L) 39.1 ± 3.6 41.1 ± 2.4 39.0 ± 3.4 37.1 ± 4.1 0.005 0.010b
Creatinine (mg/dl) 7.7 ± 2.5 8.1 ± 3.4 7.9 ± 2.3 6.6 ± 2.0 NS 0.099b,d
Cholesterol (mg/dl) 151.2 ± 33.6 181.6 ± 36.4 146.3 ± 30.0 134.0 ± 17.7 0.0001 0.0001b
Transferrin (mg/dl) 167.2 ± 36.8 188.9 ± 41.3 166.5 ± 31.8 143.3 ± 31.7 0.001 0.002b
Haemoglobin (g/dl) 11.5 ± 1.1 11.5 ± 0.70 11.5 ± 1.17 11.4 ± 1.13 NS NSb
rHuEPO dose (U/week) 11.4 ± 8.3 8.7 ± 5.0 12.0 ± 9.2 12.7 ± 7.9 NS NSb
IL-6 (pg/ml) 7.3 (0.5–152.2) 6.3 (1.5–41.5) 7.3 (0.1–152.2) 15.5 (3.4–52.0) NS NSb
Bioimpedance analysis
Fat mass (kg) 24.7 ± 9.9 27.5 ± 8.9 25.6 ± 10.2 17.2 ± 6.3 0.011 0.017b
Lean body mass (kg) 50.5 ± 10.1 51.8 ± 9.3 52.3 ± 9.5 41.2 ± 9.1 0.002 0.001b
FFM (kg) 47.6 ± 9.1 49.1 ± 8.4 49.3 ± 8.6 39.8 ± 8.4 0.002 0.0001b
Phase angle 4.9 ± 1.02 5.3 ± 1.2 5.0 ± 0.9 4.1 ± 1.0 0.006 0.0001b
MIS 7.0 ± 3.5 4.9 ± 2.1 6.3 ± 2.8 10.6 ± 3.8 0.0001 0.0001b

a
Values are expressed as mean ± SD, median and range (for non-normally distributed variables) or percentage.
b
Adjusted for gender, age, DM status and history of cardiovascular disease.
c
Hospitalization days and frequency of hospitalization are 26-month prospective data.
d
Note that P-values are shown here for comparison, despite P above 0.05.

clinical and laboratory parameters were assessed using Pearson correl-
ation coefficients or Spearman rank order correlation coefficients, in
the cases of skewed distribution of data. Alternatively, when distributions
of variables were skewed, log transformation was undertaken before as-
sessment using Pearson correlation coefficients. Multivariate regression
analysis was performed to obtain partial (adjusted) correlations (R2) con-
trolled for age, gender, history of cardiovascular (CV) disease and pres-
ence or absence of diabetes mellitus.
Survival analyses were performed using the Kaplan–Meier survival
curve and the Cox proportional hazard model. The univariate and multivari-
ate Cox regression analyses are presented as hazard ratio (HR; CI).
All statistical tests were two-sided, with a value for P < 0.05 defining
significance.
All statistical analyses were performed using SPSS software, version
16.0 (SPSS Inc, Chicago, IL).
Results
In this study, we developed and characterized a score for
the assessment of nutritional status in dialysis patients,
based solely on objectively measurable criteria. In our co-
hort, 81 prevalent HD patients (53 men and 28 women)
with a mean age 64.3 ± 11.9 years were studied. Table 2
shows the pertinent demographic, laboratory and clinical
data of these patients as a whole and for each nutritional
category, as determined by OSND: normal nutritional sta-
tus (score from 28 to 32), moderate nutritional status
(score from 23 to 27) and low nutritional status (score
<22). Over half of the patients (54.3%) had diabetes mel-
litus (DM), and nearly the same proportion had a history of
cardiovascular disease (51.9%), including myocardial in-
farction, coronary artery procedures such as angioplasty
or surgery, cerebral-vascular accident or peripheral vascu-
lar disease. Gender proportion, age, history of cardiovascu-
lar disease and dialysis vintage distribution were similar in
the three groups. The body mass index was lower across
decreasing OSND categories (P = 0.001).
Hospitalization days and hospitalization frequency in-
creased across worsening OSND categories (P = 0.014
and P = 0.022, respectively). Anthropometric measure-
ments (TSF, MAC and MAMC) as well as body compos-
ition parameters derived by BIA [fat mass (FM), lean body
mass (LBM) and FFM] showed statistically significant dif-
ferences between the three OSND groups. Phase angle
(PA)—the BIA prognostic index of morbidity and mortal-
ity [describing the relationship between the two vector
components of impedance (reactance and resistance) of
the human body to an alternating electric current] was sig-
nificantly lower in worsening OSND categories (P =
0.006). Comparison between different OSND groups ex-
2666 I. Beberashvili et al.
Table 3. Correlation coefficients between Objective Score of Nutrition on
Dialysis (OSND) and nutritional parameters (that not included in the
OSND score), demographic and hospitalization data of study population

Correlation Coefficient (r) for OSND P

Age −0.041 (−0.053) 0.719 (0.633)

Dialysis vintage −0.071 (−0.132) 0.527 (0.298)
Hospitalization frequency −0.373 (−0.338) 0.001 (0.003)
Hospitalization days −0.334 0.002 (0.002)

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(−0.347)
nPNA 0.117 (0.145) 0.307 (0.216)
Creatinine 0.068 (0.151) 0.546 (0.235)
IL-6 −0.330 (−0.212) 0.004 (0.036)
Lean body mass 0.268 (0.369) 0.018 (0.003)
Fat mass 0.322 (0.252) 0.004 (0.044)
FFM 0.263 (0.400) 0.019 (0.001)
Phase angle 0.305 (0.430) 0.006 (0.0001)
MIS −0.584 (−0.561) 0.0001 (0.0001)

In each column, the first set of values includes the unadjusted (bivariate) r
with its Pearson or Spearman (for skewed data) P-value, and the second
set (in parentheses) includes partial correlation based on a multivariate
regression analysis adjusted for case-mix (age, gender, diabetes status
and history of CV disease).
Correlation coefficient values ≥0.25 appear in bold. BMI, body mass
index; TSF, triceps skinfold thickness; MAC, mid-arm circumference;
MAMC, mid-arm muscle circumference calculated; IL-6, interleukin-6;
FFM, fat-free mass.

hibited increased albumin, cholesterol and transferrin in

the highest OSND category (P = 0.005, P = 0.0001 and
P = 0.001, respectively). MIS was significantly lower in
the patients with a higher OSND (P = 0.0001). We found
that univariate differences between laboratory and clinical
parameters of nutritional categories, as determined by
OSND, changed very little after adjusting for age, gender,
history of cardiovascular disease and DM status.
Table 3 demonstrates the bivariate and multivariate cor-
relations of OSND with some relevant demographic, clin-
ical and laboratory variables in our cohort. The OSND was
powerful for predicting prospective hospitalization. BIA-
derived parameters of body composition (LBM, FM and
FFM) correlated positively with OSND, i.e. an increased
level of this score was associated with better nutritional
status. OSND showed strong negative correlation with
the best serum inflammatory marker, interleukin 6 (IL-6)
(r = −0.330, P = 0.004), but this association was attenuated
after adjustment for age, gender and DM status. Finally,
OSND had strong reverse correlation with MIS (r =
−0.584, P = 0.0001; adjusted r2 = −0.561, P = 0.0001)
and positive correlation with phase angle (r = 0.305, P =
0.006; adjusted r2 = 0.430, P = 0.0001).
Figure 1 shows Kaplan–Meier survival analysis for the
surviving patients comparing subgroups of OSND score,
MIS and phase angle in the study population. As can be
seen, there is a significant difference in survival status
comparing each three subgroups of patients divided by
OSND (P = 0.002 by log-rank test), MIS (P = 0.030 by
log-rank test) and phase angle (P = 0.003 by log-rank test).
By using the Cox proportional hazards model, we cor-
rected these differences for potential confounding factors.
Table 4 lists hazard ratios and 95% CIs of death using Fig. 1. Kaplan–Meier proportion of surviving patients comparing
Cox proportional hazard models based on initial values at subgroups of severity according OSND (a), MIS (b) and phase angle
the start of the prospective cohort and time to death. The (c) in 81 prevalent HD patients.
Nutritional risk assessment of haemodialysis patients 2667
Table 4. Prognostic power of ONSD for all-cause mortality in 81 prevalent dialysis patients

Variable Units of decrease (↓) or increase (↑) Hazard ratio and 95% CI P-value

Unadjusted Cox regression analysis

ONSD 5 units ↓ 2.2 (1.3–3.8) 0.003
MIS 5 units ↑ 1.8 (1.2–2.8) 0.007
Phase angle 10 ↓ 2.9 (1.5–5.6) 0.001

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Multiple Cox regression analysis
OSND 5 units ↓ 2.8 (1.3–6.2) 0.009
Age 1 year ↑ 1.0 (0.9–1.1) 0.995
Gender 0 = female; 1 = male 3.6 (0.9–14.8) 0.074
DM 0 = No; 1 = Yes 4.2 (1.1–15.7) 0.036
History of CV disease 0 = No; 1 =Yes 1.2 (0.4–3.8) 0.778
IL-6 10pg/ml ↑ 1.0 (0.7–1.4) 0.988
MIS 5 units ↑ 2.2 (1.2–4.1) 0.013
Age 1 year ↑ 1.0 (0.9–1.0) 0.274
Gender 0 = female; 1 = male 3.3 (0.8–13.5) 0.102
DM 0 = No; 1 = Yes 2.5 (0.8–7.9) 0.109
History of CV disease 0 = No; 1 = Yes 1.7 (0.4–3.8) 0.798
IL-6 10pg/ml ↑ 1.0 (0.7–1.4) 0.943
Phase angle 10 ↑ 3.7 (1.7–7.9) 0.001
Age 1 year ↑ 1.0 (0.9–1.0) 0.957
Gender 0 = female; 1 = male 2.6 (0.7–9.4) 0.148
DM 0 = No; 1 =Yes 1.2 (0.5–3.4) 0.676
History of CV disease 0 = No; 1 = Yes 1.6 (0.5–4.7) 0.404
IL-6 10pg/ml ↑ 1.3 (0.9–1.8) 0.159

OSND, objective score of nutrition on dialysis; MIS, malnutrition-inflammation score; DM, diabetes mellitus; CV, cardiovascular; IL-6, interleukin-6.

model controls for age, gender, diabetes status, IL-6 and lar accident (CVA) or peripheral vascular disease (PVD)
history of cardiovascular disease at baseline to estimate requiring angioplasty, bypass or amputation and diagnosed
relative risks. The OSND showed the strong association after participants entered the study. Unfavorable OSND de-
with prospective mortality. The relative risk for death for monstrated statistically significant hazard ratios for first
each five-unit decrease in OSND was 2.8 (95% CI, 1.3 to CVA (HR = 3.5; 95% CI, 1.1 to 10.8; P = 0.028) and trend
6.2; P = 0.009). In this regard, OSND was comparable with
MIS and phase angle. The relative risk for death for each
five-unit increase in MIS was 2.2 (95% CI, 1.2 to 4.1; P =
0.013) and for each 1-unit decrease in PA was 3.7 (95% CI, Table 5. Case-mix-adjusted (for age, gender, DM status and history of
CV disease) hazard ratios of death for all components of the OSND, as
1.7 to 7.9; P = 0.001). well as the OSND itself, MIS and phase angle
Table 5 lists case-mix-adjusted hazard ratios of death for
each of the seven components of the OSND as well as the OSND components Hazard ratio (95% CI) P-value
composite OSND itself. Each OSND component was en-
tered in the Cox model as a decremental variable, consisting 1. BMI (kg/m2) 1.1 (1.0–1.2)* 0.044
of a number between 1 and 3. The MIS was divided into 2. Weight decrease (%) 1.2 (0.3–3.9) 0.811
three equal increments, and phase angle was divided into 3. TSF (mm) 1.1 (0.7–1.9) 0.669
4. MAC (cm) 1.3 (0.7–2.7) 0.424
three equal decrements as well. Three OSND components 5. Albumin (g/L) 2.2 (1.3–3.8)* 0.005
showed statistically significant hazard ratios for death: 6. Transferrin (mg/dl) 1.1 (0.7–1.9) 0.622
BMI, serum albumin and total cholesterol levels had the 7. Cholesterol (mg/dl) 2.4 (1.3–4.5)* 0.008
strongest association with mortality. However, the OSND OSND 3.6 (1.6–7.9)* 0.002
MIS 4.3 (1.6–11.7)* 0.004
was found to be a more powerful predictor of mortality than Phase angle 4.1 (1.8–9.6)* 0.001
any of its eight components (Table 5). Moreover, in this
model, OSND had as high accuracy for predicting death Each component is scored as a number between 1 and 3. Note that OSND,
(HR = 3.6; 95% CI, 1.6 to 7.9; P = 0.002) as MIS a number between 5 and 32, is divided into three equal groups (32 to 24,
(HR = 4.3; 95% CI, 1.6 to 11.7; P = 0.004) or phase angle 23 to 15 and 14 to 5). MIS, a number between 0 and 30, also is divided
(HR = 4.1; 95% CI, 1.8 to 9.6; P = 0.001). into three equal increments (0 to 10, 11 to 20, and 21 to 30). Phase angle
is divided into three decrements (7.9 to 6.0; 5.9 to 4.0 and 3.9 to 2.0).
Case-mix-adjusted hazard ratios of first cardiovascular BMI, anthropometric indexes, albumin level, transferrin level and choles-
event for OSND, MIS and phase angle for a one-unit in- terol level were each divided into three groups, in a decrement fashion and
crease within the three decrements for OSND and phase expressed as integer numbers between 1 and 3. This enabled comparison
angle and within three increments for MIS (as described of the hazard ratios of the OSND, MIS and phase angle with those of
components of OSND, as well as each with another.
above) were calculated: first cardiovascular event defined OSND, objective score of nutrition on dialysis; MIS, malnutrition-inflam-
as myocardial infarction (MI) requiring coronary artery mation score; TSF, triceps skinfold thickness; MAC, mid-arm circumfer-
procedures such as angioplasty or surgery; cerebral-vascu- ence*P < 0.05.
2668 I. Beberashvili et al.
Table 6. Adjusted multivariate correlation coefficients

Variables Hazard ratio of death Hospitalization frequency Hospitalization days Phase angle

TSF+MAC 0.194 (0.321) −0.139 (0.236) −0.178 (0.126) 0.201 (0.067)

BMI 0.070 (0.557) −0.053 (0.656) −0.078 (0.511) 0.162 (0.171)
ΔW −0.105 (0.379) 0.156 (0.187) 0.068 (0.565) −0.003 (0.979)
a (Anthropometry) = TSF+MAC+BMI+ΔW 0.224 (0.034) −0.186 (0.111) −0.258 (0.025) 0.234 (0.042)
a + Albumin 0.252 (0.029) −0.187 (0.108) −0.346 (0.002) 0.249 (0.031)
a + Transferrin 0.191 (0.101) −0.170 (0.144) −0.288 (0.012) 0.378 (0.001)

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a + Cholesterol 0.212 (0.068) −0.251 (0.030) −0.319 (0.005) 0.269 (0.020)
a + Creatinine 0.087 (0.457) −0.197 (0.090) −0.214 (0.065) 0.016 (0.894)
a + Albumin + Transferrin 0.281 (0.015) −0.174 (0.136) −0.350 (0.002) 0.379 (0.001)
a + Albumin + Cholesterol 0.306 (0.008) −0.254 (0.028) −0.392 (0.0001) 0.317 (0.006)
a + Transferrin + Cholesterol 0.252 (0.030) −0.234 (0.043) −0.335 (0.003) 0.396 (0.0001)
a + Albumin + Cholesterol + Transferrin (=OSND) 0.414 (0.0001) −0.338 (0.003) −0.347 (0.002) 0.419 (0.0001)
a + Albumin + Cholesterol + Creatinine 0.294 (0.011) −0.268 (0.020) −0.379 (0.001) 0.231 (0.047)
a + Albumin + Cholesterol + Transferrin + Creatinine 0.319 (0.005) −0.253 (0.028) −0.387 (0.001) 0.345 (0.002)

R2 and P for hazard ratios of death, hospitalization frequency, hospitalization days and phase angle derived by BIA, compared to anthropometry (in-
dicated by ‘a’), which consists of the first five components of the OSND, and its modified versions through the stepwise evolution toward the full
version of the OSND by adding three laboratory tests (albumin, transferrin and cholesterol). The 13th row is based on replacing transferrin with
creatinine in the OSND. The case-mix-adjusted correlation coefficients R2 are controlled for age, gender, diabetes status and history of CV disease.
For each multivariate R2, P is listed in parentheses.
BMI, body mass index; TSF, triceps skinfold thickness; MAC, mid-arm circumference; MAMC, mid-arm muscle circumference calculated; ΔW, de-
crease in dry weight (in past 3–6 months).

for first composite cardiovascular event (HR = 2.1; 95% CI,
1.0 to 4.5, P = 0.056). MIS was predictive only for first CVA
(HR = 4.8; 95% CI, 1.3 to 17.8; P = 0.019), whereas phase
angle had significant associations with first CVA (HR = 4.0;
95% CI, 1.2 to 13.8, P = 0.027), first PVD (HR = 4.0; 95%
CI, 1.2 to 13.4, P = 0.025) and first composite cardiovascular
event (HR = 3.4; 95% CI, 1.5 to 7.5; P = 0.003).
Table 6 demonstrates the stepwise enhancement of the
OSND model based on the addition of serum albumin,
cholesterol and transferrin levels to the anthropometric
measures. The first column represents pseudo-R2 based
on a Cox proportional hazard model [the case-mix-ad-
justed (multivariate) correlation coefficients R2 for hazard
ratios for death]. The following columns show multivariate
R2s for prospective hospitalization indices (hospitalization
days and hospitalization frequencies) and phase angle
based on multivariate linear regression models. The first
four rows show correlations between hazard ratios for
death, hospitalization indices and phase angle with the
two anthropometric measures (TSF and MAC), decrease
in dry weight and BMI, separately or combined together
(fourth row). Although, as single parameters, these mea-
surements did not exhibit correlations with clinical out-
come, they correlated significantly with hazard ratios for
death, hospitalization days and phase angle when com-
bined. The following rows show various combinations to
model a scoring system based on the addition of one or
more of the three laboratory tests (albumin, transferrin,
cholesterol) to the combination of anthropometric mea-
sures. The 12th row is the complete version of the OSND.
The 13th row represents a scoring model based on re-
placing transferrin level by creatinine level. Additional
models were also constructed and evaluated, but they did
not improve correlations with parameters that reflect clin-
ical outcome (data not shown).
The ROC curves for predicting mortality are shown in
Figure 2. The AUC for the OSND is 0.707 (P = 0.004),
demonstrating a reasonable predictive value for the score.
MIS and phase angle produced very similar AUC [0.678
(P = 0.015) and 0.739 (P = 0.001), respectively].
Discussion
The purpose of this study was to develop and evaluate a
scoring system consisting of routine objective measure-
ments for identifying nutritional risk in HD patients. Such
a quantitative and comprehensive scoring system, named
the Objective Score of Nutrition on Dialysis, was developed
by combining anthropometric measurements with three la-
boratory analyses: serum albumin, transferrin and choles-
terol levels. As this nutritional score uses only objective
information, any subjective assessments and judgments by
the examiner can therefore be avoided.
A high proportion of HD patients in this study showed
signs of malnutrition, which was mild to moderate in the
majority of patients. HD patients with malnutrition deter-
mined by OSND had a significantly lower body mass index,
serum albumin, total cholesterol and transferrin levels, as
well lean body mass, fat mass and FFM determined by
BIA. Our report also found a significant difference in an-
thropometry and MIS scores. The prevalence of malnutri-
tion within our study (about 77%) population is somewhat
higher than that found by other studies (23% to76%) per-
formed in patients with ESRD [5,28–30]. A possible ex-
planation for differences between our results and those
reported may relate to differences in the baseline demo-
graphic and some clinical characteristics of HD patients
studied: our cohort was older, with longer dialysis vintage
and with higher prevalence of diabetes. It is well known that
older age [29], long dialysis vintage [31] and presence of
diabetes mellitus [32,33] may influence the nutritional sta-
tus of HD patients either by causing a reduced nutritional
intake or by promoting catabolism.
Nutritional risk assessment of haemodialysis patients
Fig. 2. Receiver operating characteristics (ROC) curves of the OSND (a),
MIS (b) and phase angle (c) for predicting mortality.
Each component of OSND is generally accepted as a
marker of nutritional status and outcome in dialysis pa-
tients. Our findings largely agree with those of analysis
of the United States Renal Data System (USRDS) data
[34] and HEMO study [19]. These studies found that ele-
2669
vated serum albumin and BMI values were independently
associated with decreased mortality. In our study, we found
a strong association between BMI, albumin and choles-
terol with clinical outcome. It is well known that a high
body mass index is paradoxically protective and associated
with improved survival in chronic haemodialysis patients
[35,36]. Underweight itself presents an important clinical
sign of malnutrition that worsens the prognosis of chronic
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HD patients. In the recent cross-sectional study, we ob-
served that obese HD patients with BMI above 30 kg/m2
demonstrate better nutritional status even compared to nor-
mal BMI or overweight HD patients [37]. Other anthropo-
metric measures such as TSF, MAC and MAMC have been
used to assess nutritional status in maintenance HD pa-
tients [18,19,34,38]. In our study, we did not find a strong
association between separate anthropometric measures and
clinical outcome. This is consistent with numerous studies
in this field where no association has been found between
anthropometric measures and the outcome [10,39]. One of
the reasonable explanations for this may be time-
dependent associations between anthropometric indices
with subsequent mortality, with greatest effects at <6
months of follow-up: in the HEMO study, some impact
of TSF and MAC was found on relative risk of time to
mortality during the first 6 months of follow-up, but
these associations were attenuated during longer follow-up
periods [19].
Plasma albumin and cholesterol concentrations are well-
accepted markers of nutrition and have been closely re-
lated to morbidity and mortality in chronic haemodialysis
patients [14–16,29,40–42]. However, some patients treated
with maintenance dialysis have a low plasma albumin
[43,44] or cholesterol concentration [45] despite apparent-
ly adequate dialysis and protein intake, as evidence of a
negative acute-phase response. In the present study, serum
transferrin concentrations were useful in establishing the
distinction between patients with normal nutritional status
and the malnourished patient groups, but separately, they
did not predict clinical outcome. In several earlier studies,
low serum transferrin was shown to be a useful marker of
malnutrition in HD patients [17]. However, in a study by
Qureshi et al. [29], serum transferrin concentrations failed
to distinguish between patients with normal nutritional sta-
tus and the malnourished patient groups. The authors ex-
plained this by the large proportion of the patients treated
with rhEPO and intravenous or oral iron, which may inde-
pendently modify serum transferrin.
Thus, each of the anthropometric or laboratory mea-
sures of OSND have some value in nutritional evaluation
of HD patients when they were used as the single object-
ive tests, but their combination in the OSND appears to
be a more inclusive marker of all aspects of nutrition and
a strong predictor of morbidity and mortality in chronic
HD patients.
In the present study, we compared the predictive value
of OSND on prospective morbidity and mortality in chron-
ic HD patients versus two validated nutritional and prog-
nostic indicators of maintenance haemodialysis patients:
the MIS score and phase angle. The MIS has been evalu-
ated in several prospective studies and has been reported to
be a reliable prognostic indicator of morbidity and mortal-
2670
ity in the maintenance haemodialysis population [9–11]. In
a recent 5-year prospective cohort study (on 809 HD pa-
tients) by Rambod et al. [46], the MIS was demonstrated
as significantly associated with several surrogates of body
composition, health-related quality of life and death risk.
Our observations were consistent with results of these
studies: MIS correlated significantly with prospective hos-
pitalizations and was found to be a predictor of first CVA
and death in chronic HD patients.
However, the MIS requires subjective assessment and
judgment by the examiner when scoring some subjective
parameters in the HD patients, such as dietary intake or
presence of gastrointestinal symptoms. As depression, fa-
tigue and cognitive impairment are prevalent (about 27%)
in the ESRD population [12,13], subjective assessment of
such nutritional symptoms is difficult in these patients.
Nevertheless, the MIS-based nutritional evaluation was
possible in this study, as only patients without any cogni-
tive impairment and who were able to sign an informed
consent form were included.
The present study supports the previous studies showing
that PA displays very strong predictive power [21,22].
Based on Cox analysis, we showed that PA was associated
strongly with first CVA, first composite cardiovascular
event and the risk of death of our study population. This
also confirms data by Pupim et al. [47] demonstrating that
low PA conferred a 20-fold increased risk of cardiovascu-
lar death in HD patients after controlling for inflammatory
parameters. However, important limitations regarding the
reliability of bioimpedance parameters as nutritional in-
dexes must be noted. First, PA failed to reflect the overt
malnourished state in one-third of the patients who scored
as malnourished by SGA [21]. On the other hand, PA is
increased after fluid removal with dialysis [48] and is de-
creased in patients with oedema [49]. Finally, BIA is still
not used widely in all medical institutions to assess nutri-
tional state among dialysis patients.
In our study, OSND was found to have similar accuracy
with MIS and phase angle in predicting hospitalization and
mortality. Undoubtedly, correlations between the OSND
and morbidity and mortality occur because of inclusion
of known outcome markers in the scoring system. We de-
monstrated that the OSND better predicted clinical out-
come in our cohort than these surrogate nutritional
markers when used separately. However, as OSND is based
on anthropometric measurements, the limitations of these
measurements must be considered [50].
Correlation between the OSND and serum IL-6 level
was relatively strong, possibly because serum albumin
[43,44] and cholesterol [45] levels, components of the
OSND, are strongly influenced by inflammation. There-
fore, the OSND appears to represent inflammation as well
as malnutrition and consequently is an indication of the se-
verity of malnutrition–inflammation complex syndrome.
Nevertheless, some limitations of the present study
should be considered. First, this study is based on a rela-
tively small sample size and represents a single dialysis
centre, limiting any experience with generalizing these
findings. Second, this study used only an observational ap-
proach, without manipulation of exposure factors (nutri-
tion and inflammation), and, therefore, no definitive
I. Beberashvili et al.
cause-and-effect relationship can be derived for any of
the risk factors analysed. Finally, it is of utmost importance
to prospectively validate both the reproducibility and ac-
curacy of OSND as a nutritional marker versus the direct
quantification of body protein using total-body nitrogen
measurements.
Thus, OSND, a quantitative and comprehensive scoring
system for nutritional status in HD patients, is inexpensive
Downloaded from https://academic.oup.com/ndt/article-abstract/25/8/2662/1892985 by Sri Ramachandra University user on 04 December 2019
and relatively easy to perform. It is based solely on object-
ive routine measurements and appears to reliably assess the
nutritional and inflammatory status of maintenance HD pa-
tients and may also identify individuals at high risk for se-
vere morbid or fatal events. The importance of such a
scoring system is expected to be especially notable in pa-
tients with compounding conditions that prevent subjective
assessment of HD patients. Each of the OSND compo-
nents reflects a single feature of nutritional status (e.g. an-
thropometry indicates body composition, albumin and
transferrin—body protein stores; cholesterol is an indicator
of energy intake, etc); thus, when taken together, they rep-
resent a powerful tool in the assessment of overall nutri-
tional status of chronic HD patients that is strongly
associated with clinical outcome.
Conflict of interest statement. None declared.
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Received for publication: 7.11.09; Accepted in revised form: 14.1.10