DOI: 10.1111/sdi.

12917

ORIGINAL ARTICLE

Assessment of nutritional status in maintenance hemodialysis

patients: A multicenter cross-sectional study in Iran

Zahra Akhlaghi1 | Farzaneh Sharifipour1 | Mohsen Nematy1 | Mohammad Safarian1 |

Mahsa Malekahmadi2 | Bahareh Barkhidarian1 | Abdolreza Norouzy1

1
Department of Nutrition, Faculty of
Medicine, Mashhad University of Medical
Sciences, Mashhad, Iran
2
Research Center for Gastroenterology
and Liver Disease, Shahid Beheshti
University of Medical Sciences, Tehran,
Iran
Correspondence
Abdolreza Norouzy, Mashhad University
of Medical Sciences (MUMS), Paradise
Daneshgah , Azadi Square, Post code
91779-48564 Mashhad, Iran.
Email: norouzya@mums.ac.ir
Funding information
Mashhad University of Medical Sciences
Abstract
Introduction: Protein-energy wasting (PEW) is common in hemodialysis patients and
is linked with a high rate of morbidity and mortality. Regarding importance of nutri-
tion in these patients, a recent study was administered to evaluate the nutritional
status of hemodialysis patients.
Materials: In this cross-sectional study 540 HD patients from 15 dialysis centers
were evaluated. The nutritional status of the patients was determined by Subjective
Global Assessment (SGA), Dialysis Malnutrition Score (DMS), and Malnutrition
Inflammation Score (MIS). Their dietary intakes were assessed using a Food Frequency
Questionnaire (FFQ).
Result: Based on DMS, 66.7% of HD patients were well nourished and the prevalence
of mild-to-moderate and severe PEW were 32.4% and 0.9% in HD patients, respec-
tively. Based on MIS, 65.2% of HD patients were well nourished and the prevalence of
mild-to-moderate and severe PEW was 34.0%. The prevalence of mild-to-moderate
and severe malnutrition based on SGA was 35.0% and 1.1%, respectively. Energy and
protein intake in 85.6% and 80.6% of patients respectively were less than the mini-
mum recommended amount.
Conclusion: HD patients are at risk of malnutrition and in this regard training the
patient, periodic assessment of nutritional status, and referring them to a dietitian
seems necessary.

1 | I NTRO D U C TI O N result in increased length of hospital stays and death in HD pa-

Malnutrition in HD patients is due to dietary limitation, anorexia,
nutrient wastage during dialysis, and rising catabolism due to in-
1-4
flammatory cytokines. Inadequate dietary intake due to dietary
restrictions and poor appetite is related to protein-energy wasting
(PEW). Many factors are directly contributed to the renal failure, in-
cluding increased basal metabolic rate (BMR), persistent inflamma-
tion, metabolic acidosis, endocrine diseases, and the dialysis process
itself.5
Protein-energy malnutrition occurs commonly in HD patients
and is linked to increased morbidity and mortality. 5 PEW contribute
to major adverse events and significant comorbid condition and
tients. 6 Poor nutritional status in HD patients has been shown in
many studies.7-11 In some studies, the prevalence of protein-energy
malnutrition is estimated at 51 to 70 percent in HD patients.11,12
Assessment of nutritional status is an important issue in identi-
fying PEW in HD patients.14 Evaluation of protein and energy intake
and nutritional status of HD patients are complex topics.15,16 The
association between the high prevalence of PEW and morbidity and
mortality in HD patients requires special attention to choose the ap-
propriate criteria or method to evaluate nutritional status. Due to a
lack of gold standard, use of multiple subjective and objective meth-
ods are recommended.17,18 This study was performed to evaluate
the nutritional status of HD patients in the Iranian population using

Seminars in Dialysis. 2020;00:1–6. wileyonlinelibrary.com/journal/sdi© 2020 Wiley Periodicals LLC. | 1

2 |
Subjective Global Assessment (SGA), Dialysis Malnutrition Score
(DMS), Malnutrition Inflammation Score (MIS), and dietary intake
assessment.
2 | M ATE R I A L S A N D M E TH O DS
This cross-sectional, descriptive-analytic study was formed on
540 patients with ESRD (End-Stage Renal Disease) undergoing
maintenance hemodialysis in 15 hemodialysis centers in Iran. The
inclusion criteria included more than 40 years of age and being
on HD for more than 6 months. The exclusion criteria included
HIV infection, HBV and HCV infection, and malignancy. The study
population composed of 540 patients. The study protocol was
approved by the Ethics Committee of the Mashhad University of
Medical Sciences. Written informed consent was taken from all
participants.
Baseline data such as age, gender, the duration of hemodialysis
(year), and biochemical markers were extracted. Body dry weight
and height and mid-arm circumference (MAC) were measured 10 to
20 minutes after termination of the dialysis session. All anthropo-
metric measurements were performed by a dietician. Dry postdialy-
sis weight was applied to estimate energy and protein requirements.
Dialysis adequacy according to Kt/V index was determined using
clinical information including predialysis blood urea nitrogen (BUN)
concentration, postdialysis BUN, the dialysis session length, postdi-
1
alysis weight, and ultrafiltration volume.
2.1 | Subjective global assessment
The Subjective Global Assessment (SGA) is a semi-quantitative scor-
ing system including medical and nutritional history and physical ex-
amination.8,9 The medical and nutritional history includes five items:
weight loss in the last 6 months, gastrointestinal (GI) symptoms, di-
etary intake, functional capacity, and comorbidities. Each of these
items is classified between A and C and indicates well nourished to
severely malnourished. The physical examination consists of three
items: subcutaneous fat and muscle wasting. The third component
of physical examination is the presence of edema or ascites that is
not applied for HD patients. The score of these two components
is from 0 to 3 points, indicating normal to severely abnormal. The
overall score of SGA represents three categories: A: well nourished,
B: mild-to-moderate malnutrition, and C: severe malnutrition.19
2.2 | Dialysis malnutrition score
Dialysis Malnutrition Score (DMS) includes seven items of the con-
ventional SGA: weight change, food intake, functional capacity,
GI symptoms, comorbidities, subcutaneous fat, number of dialysis
therapy years, and signs of muscle wasting.10 Each item gets a score
ranging from 1 (normal) to 5 (severely abnormal). DMS from 1 to 7
ZAHRA et al.
indicates the normal nutritional status to severe malnutrition (pro-
tein-energy malnutrition).19
2.3 | Malnutrition inflammation score
Malnutrition Inflammation Score (MIS)contains the seven DMS
items plus three new items as follows, body mass index (BMI), serum
albumin level, and total iron-binding capacity (TIBC). MIS consists
of 10 items, each item score ranging, from 0 (normal) to 3 (severely
abnormal). The overall scores of all 10 MIS items indicate 0 (normal)
to 30 (severely malnourished). 20
2.4 | Dietary assessment
The dietary intakes in HD patients were assessed using a Food
Frequency Questionnaire (FFQ) of 160 items which was designed
and validated for the Iranian population. 21-23
2.5 | Statistical analysis
Data were analyzed using SPSS software version 16.0 (SPSS, Inc)
All quantitative parameters had nonnormal distribution based on
the Kolmogorov-Smirnov test. We used the Mann-Whitney test to
compare quantitative parameters between two groups and Kruskal-
Wallis Tests among more than two groups. A chi-squared test was
used to determine associations between qualitative variables.
(P-value < 0.05) was considered statistically significant.
3 | R E S U LT S
Five hundred and forty HD patients have participated in this study.
The characteristics of HD patients are shown in Table 1. Among the
patients, 27.6% had <1.2 Kt/V dialysis adequacy and 72.4% had ≥1.2
Kt/V dialysis adequacy. The mean BMI was 23.8 ± 4.7 kg/m2 and MAC
was 27/0 ± 9.7 cm. The serum level of albumin was 4.0 ± 0.4 g/dL.
Underlying causes of renal failure follow as, diabetes (46%), hy-
pertension (30%), polycystic kidney disease (5%), urinary infection
(4%), glomerulonephritis (0.7%), neurogenic bladder (0.4%), reflux
nephropathy (0.3%), and idiopathic/nondiagnosed causes (12%).
Ninety-three percent of participating patients had hemodialysis
therapy three times a week (4 hours per session), 7% of patients had
twice weekly (4 hours per session).
Fifty-seven percent of patients during and after dialysis reported
some type of complications. Most of the complaints raised by pa-
tients were hypotension (29%), headache (13%), muscle cramps (7%),
hypertension (5%), nausea (2%), lethargy (1%), and chest pain (0.2%).
The daily energy and protein intake in hemodialysis patients
shown in Table 2. 86% and 81% of HD patients had dietary en-
ergy and protein intake lower than recommended, respectively.
ZAHRA et al. | 3

TA B L E 1 Characteristics of hemodialysis patients TA B L E 4 Prevalence of Protein-Energy Malnutrition in

hemodialysis patients with SGAa. DMSb and MISc score
All patients
Characteristics (n = 540) (%) Parameter score Classification based on scores n = 540 (%)

Age (y) SGA Well-nourished 345 (63.9)

18-40 99 (18.3) Mild-to-moderate malnutrition 189 (35.0)
41-60 244 (45.2) Severe malnutrition 6 (1.1)
>60 197 (36.5) DMS Well-nourished 360 (66.7)
Sex Mild-to-moderate malnutrition 175 (32.4)
Men 285 (52.8) Severe malnutrition 5 (0.9)
Women 255 (47.2) MIS Well-nourished 352 (65.2)
Dialysis vintage (y) Mild-to-moderate malnutrition 188 (34.8)
≤1 144 (26.7) Severe malnutrition 0
1-5 300 (55.6) Abbreviations: DMS, Dialysis Malnutrition Score; MIS, Malnutrition
5-10 66 (12.2) Inflammation Score; SGA, subjective global assessment.
>10 30 (5.6)
Dialysis adequacy (Kt/V)
<1.2 137 (27.6)
nourished and 32% and 0.9% of patients had mild-to-moderate and
≥1.2 359 (72.4)
severe PEW, respectively. Based on MIS, 65% of HD patients were
BMI (kg/m2) 23.8 ± 4.7
well nourished and 34.0% and 0% of patients had mild-to-moderate
MAC (cm) 27.0 ± 9.7
and severe PEW, respectively (Table 4).
Serum Albumin (g/dL) 4.0 ± 0.4
There were significant associations between nutrition sta-
Note: BMI.MAC and Serum Albumin are presented as mean ± SD. tus (SGA score) with the age of patients (P < .001) and their HD
vintage (P < .001) (Table 5). No significant associations were
TA B L E 2 The daily energy and protein intake in hemodialysis detected between the prevalence of PEW (SGA score) with sex
patients
and dialysis adequacy (Table 5). There was a significant associa-
Recommended tion between dietary protein intake and the prevalence of PEW
Food component n = 540 (%) values (SGA score) (P < .001) (Table 5). The association between dietary
Energy (kcal/kg/d) energy intake and SGA of patients was marginally significant
<Recommended intake 459 (85.6) <60 y: 35 kcal/d (P < .001) (Table 5).
≥Recommended intake 77 (14.4) ≥60 y: 30-35 kcal/d
Protein (g/kg/d)
<Recommended intake 431 (80.6) ≥1.2 g/d
4 | DISCUSSION
≥Recommended intake 104 (19.4)
The objective of this study was to evaluate the nutritional sta-
tus of HD patients based on Subjective Global Assessment,
TA B L E 3 Mean ± SD energy and protein intake in hemodialysis Dialysis Malnutrition Score, and Malnutrition Inflammation Score
patients estimated via food frequency questionnaire methods.
Protein and energy intake Mean ± SD This study showed that in adult HD patients in Iran, based on
SGA 35% had mild-to-moderate malnutrition. By DMS 32% had
Energy intake (Kcal/kg/d) 1535 ± 858
mild-to-moderate malnutrition and according to MIS, 35% had
Energy intake (Kcal/d) 26.3 ± 27.0
mild-to-moderate malnutrition. Severe malnutrition by SGA, DMS,
Protein intake (g/d) 54.5 ± 30.0
and MIS was 1.1%, 0.9% and 0% respectively. This finding is in agree-
Protein intake (g/kg/d) 0.9 ± 0.8
ment with those of smaller studies in Iran. Tabibi et al, in a study from
Tehran-Iran, showed that 60.5% of HD patients had mild-to-mod-
The mean (±SD) protein and energy intake of patients shown in erate PEW and 1% had severe PEW. 24 In the study by Saran et al,
Table 3. Mean (±SD) protein and energy intakes in HD patients were the prevalence of mild-to-moderate and severe PEW was 24% and
26.3 ± 27.0 kcal/kg/d and 0.9 ± 0.8 g/kg/d, respectively, which were 8%, respectively. 25 Desbrow et al, in a study from Australia, reported
less than the recommended levels. that based on a PG-SGA, 20% of HD patients had moderate PEW. 26
According to SGA, 64% of HD patients were well nourished In a study conducted in Baghdad Iraq, Al-Seady et al reported the
and 35.0% and 1.1% of patients had mild-to-moderate and severe prevalence of mild and moderate-to-severe PEW to be 45.9% and
PEW, respectively. Based on DMS, 67% of HD patients were well 17.6%, respectively. 27
4 | ZAHRA et al.

TA B L E 5 Prevalence of protein-energy
Well Mild-to-moderate Severe
malnutrition by sex, age dialysis vintage,
Variables nourished malnutrition malnutrition P-Value
dialysis adequacy, protein, and energy
Sex intake in hemodialysis patients based on
Men 189 (66.3) 93 (32.6) 3 (1.1) NS SGA

Women 156 (61.2) 96 (37.6) 3 (1.2)

Age
<60 230 (68.9) 100 (29.9) 4 (1.2) ˂.001
≥60 115 (55.8) 89 (43.2) 2 (1.0)
Dialysis vintage (year)
<5 293 (66./0) 150 (33.8) 1 (0.2) ˂.001
≥5 52 (54.2) 39 (40.6) 5 (5.2)
Dialysis adequacy (Kt/V)
<1/2 85 (62.0) 51 (37.2) 1 (0.7) NS
≥1/2 230 (64.1) 125 (34.8) 5 (1.7)
Energy intake (kcal/kg/d)
<Recommended intake 303 (66.0) 153 (33.3) 3 (7%) .002
≥Recommended intake 38 (94.4) 36 (46.8) 3 (3.9)
Protein intake (g/kg/d)
<1/2 228 (66.8) 137 (31.8) 6 (1.4) .003
≥1/2 53 (51/0) 51 (49.0) 0 (0)

Abbreviation: SGA, subjective global assessment.

Energy and protein intakes in 85.6% and 80.6% of patients
on dialysis were less than the minimum recommended amount.
Mean (±SD) energy and protein intakes in HD patients were
26.3 ± 27.0 kcal/kg/d and 0.9 ± 0.8g/kg/d, respectively, which were
less than recommended intakes of energy and protein.1,28 These
findings are similar to those of previous studies. Tabibi et al in a
study in Tehran-Iran showed that 88% and 84.5% of HD patients
had inadequate energy and protein intakes, respectively. 24 In a
study from the United States, in the study of Kalantar-Zadeh et al,
the mean of energy intake was 26.4 ± 15.3 kcal/kg/d and protein
intake was 0.88 ± 0.57 g/kg/d in HD patients.13 In Bossola et al’s
study, the mean of energy intake was 25 ± 10.1 kcal/kg/d and pro-
tein intake was 0.64 ± 0.4 g/kg/d.9
In HD patients, intake of dietary energy and protein lower than
recommended results in malnutrition and poor quality of life and en-
hanced morbidity and mortality. The most important reason for not
receiving enough dietary nutrients is anorexia. Anorexia may be due
to serum amino acid patterns, inflammation, uremic toxins, changes
in the level of hormones and neurotransmitters related to appetite,
and underlying diseases such as infections and emotional disorders,
especially depression, which is common in patients with chronic
renal disorders. Other reasons for energy-protein malnutrition in HD
patients are inability to provide food physically and economically,
also underlying illnesses such as diabetes leads to further dietary
restrictions. Dental problems and hyperkalemia or hyperphosphate-
1
mia reduce food consumption.
85.6% and 80.6% of patients had dietary energy and protein
intake lower than recommended values, respectively. This finding
revealed a significant association between the prevalence of PEW
with dietary intakes of energy (P < .002) and protein (P < .003).
Energy and protein intakes in patients with malnutrition were
significantly lower than other patients, which is similar to the
findings of As'habi et al.1 In our study, there was no significant
association between the prevalence of PEW (SGA score) and sex
(P = .463). Besides this study showed that there is no significant
association between SGA score and dialysis adequacy (P > .05).
We found a significant association between the patient's age and
the SGA score (P = .000). Mild and moderate malnutrition was
significantly higher in HD patients with age ≥ 60 years, compared
to patients with age less than 60 years. Also, the association be-
tween SGA score and the patient's age was marginally significant.
Some factors such as the high prevalence of infections, emotional
disorders, especially depression, physical or economic inability to
provide food, and dental problems in the elderly can explain the
reason for this relationship.1 This finding is similar to the finding
of As'habi et al.1 We found no significant association between
dialysis vintage and SGA score. The prevalence of malnutrition
was higher in HD patients who had dialysis vintage ≥5 years and
was significantly higher compared with those with dialysis vin-
tage <5 years. This could be a result of continuous loss of amino
acid, protein, water-soluble vitamins, and minerals through he-
modialysis, while this losing is not compensated, and the patient
will have become malnourished in long term. This finding is in dis-
agreement with that of As'habi et al.1 The relationship between
serum albumin levels and malnutrition was not significant in our
study, which is consistent with the findings of Espahbodi et al. 29
ZAHRA et al. | 5

The results of our study were probably due to the influence of
other factors, including proteinuria, in patients with renal insuf-
ficiency. Also, because albumin is an acute-phase protein and
varying degrees of vascular inflammation existed in HD patients,
serum albumin levels may be changed. 29 Based on our findings,
which demonstrated a high prevalence of malnutrition in HD pa-
tients and the notability of malnutrition as a prognostic factor in
these patients, we recommend nutritional training of patients and
regular patient counseling with a dietitian, to prevent, diagnose,
and treat malnutrition.
AC K N OW L E D G M E N T S
This study was supported by the Mashhad University of Medical
Sciences of Iran. The authors thank the staff of the Mashhad he-
modialysis centers and the staff of the nutrition department of
Mashhad University of Medical Science for their assistance.
C O N FL I C T O F I N T E R E S T
The authors have disclosed that they have no significant relation-
ships with, or financial interest in, any commercial companies per-
taining to this article.
ORCID
Zahra Akhlaghi https://orcid.org/0000-0002-9529-021X
Farzaneh Sharifipour https://orcid.org/0000-0003-1536-5451
Mohsen Nematy https://orcid.org/0000-0001-5919-0687
Mohammad Safarian https://orcid.org/0000-0002-0583-0412
Mahsa Malekahmadi https://orcid.org/0000-0002-6707-6929
Bahareh Barkhidarian https://orcid.org/0000-0002-3604-4406
Abdolreza Norouzy https://orcid.org/0000-0001-6740-5502
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